diff --git a/packages/react-client/src/ReactFlightClient.js b/packages/react-client/src/ReactFlightClient.js
index 0e22e3f294fb5..61a67bce9d803 100644
--- a/packages/react-client/src/ReactFlightClient.js
+++ b/packages/react-client/src/ReactFlightClient.js
@@ -341,6 +341,11 @@ export type FindSourceMapURLCallback = (
 
 export type DebugChannelCallback = (message: string) => void;
 
+export type DebugChannel = {
+  hasReadable: boolean,
+  callback: DebugChannelCallback | null,
+};
+
 type Response = {
   _bundlerConfig: ServerConsumerModuleMap,
   _serverReferenceConfig: null | ServerManifest,
@@ -362,7 +367,7 @@ type Response = {
   _debugRootStack?: null | Error, // DEV-only
   _debugRootTask?: null | ConsoleTask, // DEV-only
   _debugFindSourceMapURL?: void | FindSourceMapURLCallback, // DEV-only
-  _debugChannel?: void | DebugChannelCallback, // DEV-only
+  _debugChannel?: void | DebugChannel, // DEV-only
   _blockedConsole?: null | SomeChunk<ConsoleEntry>, // DEV-only
   _replayConsole: boolean, // DEV-only
   _rootEnvironmentName: string, // DEV-only, the requested environment name.
@@ -404,16 +409,16 @@ function getWeakResponse(response: Response): WeakResponse {
   }
 }
 
-function cleanupDebugChannel(debugChannel: DebugChannelCallback): void {
-  // When a Response gets GC:ed because nobody is referring to any of the objects that lazily
-  // loads from the Response anymore, then we can close the debug channel.
-  debugChannel('');
+function closeDebugChannel(debugChannel: DebugChannel): void {
+  if (debugChannel.callback) {
+    debugChannel.callback('');
+  }
 }
 
 // If FinalizationRegistry doesn't exist, we cannot use the debugChannel.
 const debugChannelRegistry =
   __DEV__ && typeof FinalizationRegistry === 'function'
-    ? new FinalizationRegistry(cleanupDebugChannel)
+    ? new FinalizationRegistry(closeDebugChannel)
     : null;
 
 function readChunk<T>(chunk: SomeChunk<T>): T {
@@ -1007,7 +1012,7 @@ export function reportGlobalError(
     if (debugChannel !== undefined) {
       // If we don't have any more ways of reading data, we don't have to send any
       // more neither. So we close the writable side.
-      debugChannel('');
+      closeDebugChannel(debugChannel);
       response._debugChannel = undefined;
     }
   }
@@ -1494,8 +1499,8 @@ function waitForReference<T>(
 ): T {
   if (
     __DEV__ &&
-    // TODO: This should check for the existence of the "readable" side, not the "writable".
-    response._debugChannel === undefined
+    (response._debugChannel === undefined ||
+      !response._debugChannel.hasReadable)
   ) {
     if (
       referencedChunk.status === PENDING &&
@@ -2262,15 +2267,16 @@ function parseModelString(
       case 'Y': {
         if (__DEV__) {
           if (value.length > 2) {
-            const debugChannel = response._debugChannel;
-            if (debugChannel) {
+            const debugChannelCallback =
+              response._debugChannel && response._debugChannel.callback;
+            if (debugChannelCallback) {
               if (value[2] === '@') {
                 // This is a deferred Promise.
                 const ref = value.slice(3); // We assume this doesn't have a path just id.
                 const id = parseInt(ref, 16);
                 if (!response._chunks.has(id)) {
                   // We haven't seen this id before. Query the server to start sending it.
-                  debugChannel('P:' + ref);
+                  debugChannelCallback('P:' + ref);
                 }
                 // Start waiting. This now creates a pending chunk if it doesn't already exist.
                 // This is the actual Promise we're waiting for.
@@ -2280,7 +2286,7 @@ function parseModelString(
               const id = parseInt(ref, 16);
               if (!response._chunks.has(id)) {
                 // We haven't seen this id before. Query the server to start sending it.
-                debugChannel('Q:' + ref);
+                debugChannelCallback('Q:' + ref);
               }
               // Start waiting. This now creates a pending chunk if it doesn't already exist.
               const chunk = getChunk(response, id);
@@ -2358,7 +2364,7 @@ function ResponseInstance(
   findSourceMapURL: void | FindSourceMapURLCallback, // DEV-only
   replayConsole: boolean, // DEV-only
   environmentName: void | string, // DEV-only
-  debugChannel: void | DebugChannelCallback, // DEV-only
+  debugChannel: void | DebugChannel, // DEV-only
 ) {
   const chunks: Map<number, SomeChunk<any>> = new Map();
   this._bundlerConfig = bundlerConfig;
@@ -2420,10 +2426,14 @@ function ResponseInstance(
     this._rootEnvironmentName = rootEnv;
     if (debugChannel) {
       if (debugChannelRegistry === null) {
-        // We can't safely clean things up later, so we immediately close the debug channel.
-        debugChannel('');
+        // We can't safely clean things up later, so we immediately close the
+        // debug channel.
+        closeDebugChannel(debugChannel);
         this._debugChannel = undefined;
       } else {
+        // When a Response gets GC:ed because nobody is referring to any of the
+        // objects that lazily load from the Response anymore, then we can close
+        // the debug channel.
         debugChannelRegistry.register(this, debugChannel);
       }
     }
@@ -2451,7 +2461,7 @@ export function createResponse(
   findSourceMapURL: void | FindSourceMapURLCallback, // DEV-only
   replayConsole: boolean, // DEV-only
   environmentName: void | string, // DEV-only
-  debugChannel: void | DebugChannelCallback, // DEV-only
+  debugChannel: void | DebugChannel, // DEV-only
 ): WeakResponse {
   return getWeakResponse(
     // $FlowFixMe[invalid-constructor]: the shapes are exact here but Flow doesn't like constructors
@@ -3545,8 +3555,8 @@ function resolveDebugModel(
   if (
     __DEV__ &&
     ((debugChunk: any): SomeChunk<any>).status === BLOCKED &&
-    // TODO: This should check for the existence of the "readable" side, not the "writable".
-    response._debugChannel === undefined
+    (response._debugChannel === undefined ||
+      !response._debugChannel.hasReadable)
   ) {
     if (json[0] === '"' && json[1] === '$') {
       const path = json.slice(2, json.length - 1).split(':');
diff --git a/packages/react-server-dom-esm/src/client/ReactFlightDOMClientBrowser.js b/packages/react-server-dom-esm/src/client/ReactFlightDOMClientBrowser.js
index bd0e0dfa1436c..d61f132310547 100644
--- a/packages/react-server-dom-esm/src/client/ReactFlightDOMClientBrowser.js
+++ b/packages/react-server-dom-esm/src/client/ReactFlightDOMClientBrowser.js
@@ -10,9 +10,10 @@
 import type {Thenable} from 'shared/ReactTypes.js';
 
 import type {
-  Response as FlightResponse,
-  FindSourceMapURLCallback,
+  DebugChannel,
   DebugChannelCallback,
+  FindSourceMapURLCallback,
+  Response as FlightResponse,
 } from 'react-client/src/ReactFlightClient';
 
 import type {ReactServerValue} from 'react-client/src/ReactFlightReplyClient';
@@ -72,6 +73,19 @@ function createDebugCallbackFromWritableStream(
 }
 
 function createResponseFromOptions(options: void | Options) {
+  const debugChannel: void | DebugChannel =
+    __DEV__ && options && options.debugChannel !== undefined
+      ? {
+          hasReadable: options.debugChannel.readable !== undefined,
+          callback:
+            options.debugChannel.writable !== undefined
+              ? createDebugCallbackFromWritableStream(
+                  options.debugChannel.writable,
+                )
+              : null,
+        }
+      : undefined;
+
   return createResponse(
     options && options.moduleBaseURL ? options.moduleBaseURL : '',
     null,
@@ -89,12 +103,7 @@ function createResponseFromOptions(options: void | Options) {
     __DEV__ && options && options.environmentName
       ? options.environmentName
       : undefined,
-    __DEV__ &&
-      options &&
-      options.debugChannel !== undefined &&
-      options.debugChannel.writable !== undefined
-      ? createDebugCallbackFromWritableStream(options.debugChannel.writable)
-      : undefined,
+    debugChannel,
   );
 }
 
diff --git a/packages/react-server-dom-esm/src/client/ReactFlightDOMClientNode.js b/packages/react-server-dom-esm/src/client/ReactFlightDOMClientNode.js
index 206ba2faea9f1..3500b3f41f2b9 100644
--- a/packages/react-server-dom-esm/src/client/ReactFlightDOMClientNode.js
+++ b/packages/react-server-dom-esm/src/client/ReactFlightDOMClientNode.js
@@ -10,8 +10,9 @@
 import type {Thenable, ReactCustomFormAction} from 'shared/ReactTypes.js';
 
 import type {
-  Response,
+  DebugChannel,
   FindSourceMapURLCallback,
+  Response,
 } from 'react-client/src/ReactFlightClient';
 
 import type {Readable} from 'stream';
@@ -88,6 +89,14 @@ function createFromNodeStream<T>(
   moduleBaseURL: string,
   options?: Options,
 ): Thenable<T> {
+  const debugChannel: void | DebugChannel =
+    __DEV__ && options && options.debugChannel !== undefined
+      ? {
+          hasReadable: options.debugChannel.readable !== undefined,
+          callback: null,
+        }
+      : undefined;
+
   const response: Response = createResponse(
     moduleRootPath,
     null,
@@ -103,6 +112,7 @@ function createFromNodeStream<T>(
     __DEV__ && options && options.environmentName
       ? options.environmentName
       : undefined,
+    debugChannel,
   );
 
   if (__DEV__ && options && options.debugChannel) {
diff --git a/packages/react-server-dom-parcel/src/client/ReactFlightDOMClientBrowser.js b/packages/react-server-dom-parcel/src/client/ReactFlightDOMClientBrowser.js
index c118077a08662..808b49d9d75d0 100644
--- a/packages/react-server-dom-parcel/src/client/ReactFlightDOMClientBrowser.js
+++ b/packages/react-server-dom-parcel/src/client/ReactFlightDOMClientBrowser.js
@@ -9,8 +9,9 @@
 
 import type {Thenable} from 'shared/ReactTypes.js';
 import type {
-  Response as FlightResponse,
+  DebugChannel,
   DebugChannelCallback,
+  Response as FlightResponse,
 } from 'react-client/src/ReactFlightClient';
 import type {ReactServerValue} from 'react-client/src/ReactFlightReplyClient';
 import type {ServerReferenceId} from '../client/ReactFlightClientConfigBundlerParcel';
@@ -99,6 +100,39 @@ function createDebugCallbackFromWritableStream(
   };
 }
 
+function createResponseFromOptions(options: void | Options) {
+  const debugChannel: void | DebugChannel =
+    __DEV__ && options && options.debugChannel !== undefined
+      ? {
+          hasReadable: options.debugChannel.readable !== undefined,
+          callback:
+            options.debugChannel.writable !== undefined
+              ? createDebugCallbackFromWritableStream(
+                  options.debugChannel.writable,
+                )
+              : null,
+        }
+      : undefined;
+
+  return createResponse(
+    null, // bundlerConfig
+    null, // serverReferenceConfig
+    null, // moduleLoading
+    callCurrentServerCallback,
+    undefined, // encodeFormAction
+    undefined, // nonce
+    options && options.temporaryReferences
+      ? options.temporaryReferences
+      : undefined,
+    __DEV__ ? findSourceMapURL : undefined,
+    __DEV__ ? (options ? options.replayConsoleLogs !== false : true) : false, // defaults to true
+    __DEV__ && options && options.environmentName
+      ? options.environmentName
+      : undefined,
+    debugChannel,
+  );
+}
+
 function startReadingFromUniversalStream(
   response: FlightResponse,
   stream: ReadableStream,
@@ -176,28 +210,7 @@ export function createFromReadableStream<T>(
   stream: ReadableStream,
   options?: Options,
 ): Thenable<T> {
-  const response: FlightResponse = createResponse(
-    null, // bundlerConfig
-    null, // serverReferenceConfig
-    null, // moduleLoading
-    callCurrentServerCallback,
-    undefined, // encodeFormAction
-    undefined, // nonce
-    options && options.temporaryReferences
-      ? options.temporaryReferences
-      : undefined,
-    __DEV__ ? findSourceMapURL : undefined,
-    __DEV__ ? (options ? options.replayConsoleLogs !== false : true) : false, // defaults to true
-    __DEV__ && options && options.environmentName
-      ? options.environmentName
-      : undefined,
-    __DEV__ &&
-      options &&
-      options.debugChannel !== undefined &&
-      options.debugChannel.writable !== undefined
-      ? createDebugCallbackFromWritableStream(options.debugChannel.writable)
-      : undefined,
-  );
+  const response: FlightResponse = createResponseFromOptions(options);
   if (
     __DEV__ &&
     options &&
@@ -226,28 +239,7 @@ export function createFromFetch<T>(
   promiseForResponse: Promise<Response>,
   options?: Options,
 ): Thenable<T> {
-  const response: FlightResponse = createResponse(
-    null, // bundlerConfig
-    null, // serverReferenceConfig
-    null, // moduleLoading
-    callCurrentServerCallback,
-    undefined, // encodeFormAction
-    undefined, // nonce
-    options && options.temporaryReferences
-      ? options.temporaryReferences
-      : undefined,
-    __DEV__ ? findSourceMapURL : undefined,
-    __DEV__ ? (options ? options.replayConsoleLogs !== false : true) : false, // defaults to true
-    __DEV__ && options && options.environmentName
-      ? options.environmentName
-      : undefined,
-    __DEV__ &&
-      options &&
-      options.debugChannel !== undefined &&
-      options.debugChannel.writable !== undefined
-      ? createDebugCallbackFromWritableStream(options.debugChannel.writable)
-      : undefined,
-  );
+  const response: FlightResponse = createResponseFromOptions(options);
   promiseForResponse.then(
     function (r) {
       if (
diff --git a/packages/react-server-dom-parcel/src/client/ReactFlightDOMClientEdge.js b/packages/react-server-dom-parcel/src/client/ReactFlightDOMClientEdge.js
index 03c050f4cba3b..54c72968c22fe 100644
--- a/packages/react-server-dom-parcel/src/client/ReactFlightDOMClientEdge.js
+++ b/packages/react-server-dom-parcel/src/client/ReactFlightDOMClientEdge.js
@@ -9,7 +9,10 @@
 
 import type {Thenable, ReactCustomFormAction} from 'shared/ReactTypes.js';
 
-import type {Response as FlightResponse} from 'react-client/src/ReactFlightClient';
+import type {
+  DebugChannel,
+  Response as FlightResponse,
+} from 'react-client/src/ReactFlightClient';
 import type {ReactServerValue} from 'react-client/src/ReactFlightReplyClient';
 
 import {
@@ -81,6 +84,14 @@ export type Options = {
 };
 
 function createResponseFromOptions(options?: Options) {
+  const debugChannel: void | DebugChannel =
+    __DEV__ && options && options.debugChannel !== undefined
+      ? {
+          hasReadable: options.debugChannel.readable !== undefined,
+          callback: null,
+        }
+      : undefined;
+
   return createResponse(
     null, // bundlerConfig
     null, // serverReferenceConfig
@@ -96,6 +107,7 @@ function createResponseFromOptions(options?: Options) {
     __DEV__ && options && options.environmentName
       ? options.environmentName
       : undefined,
+    debugChannel,
   );
 }
 
diff --git a/packages/react-server-dom-parcel/src/client/ReactFlightDOMClientNode.js b/packages/react-server-dom-parcel/src/client/ReactFlightDOMClientNode.js
index 42e71c2c8a764..b513fd3faca33 100644
--- a/packages/react-server-dom-parcel/src/client/ReactFlightDOMClientNode.js
+++ b/packages/react-server-dom-parcel/src/client/ReactFlightDOMClientNode.js
@@ -8,7 +8,7 @@
  */
 
 import type {Thenable, ReactCustomFormAction} from 'shared/ReactTypes.js';
-import type {Response} from 'react-client/src/ReactFlightClient';
+import type {DebugChannel, Response} from 'react-client/src/ReactFlightClient';
 import type {Readable} from 'stream';
 
 import {
@@ -82,6 +82,14 @@ export function createFromNodeStream<T>(
   stream: Readable,
   options?: Options,
 ): Thenable<T> {
+  const debugChannel: void | DebugChannel =
+    __DEV__ && options && options.debugChannel !== undefined
+      ? {
+          hasReadable: options.debugChannel.readable !== undefined,
+          callback: null,
+        }
+      : undefined;
+
   const response: Response = createResponse(
     null, // bundlerConfig
     null, // serverReferenceConfig
@@ -95,6 +103,7 @@ export function createFromNodeStream<T>(
     __DEV__ && options && options.environmentName
       ? options.environmentName
       : undefined,
+    debugChannel,
   );
 
   if (__DEV__ && options && options.debugChannel) {
diff --git a/packages/react-server-dom-turbopack/src/__tests__/ReactFlightTurbopackDOMBrowser-test.js b/packages/react-server-dom-turbopack/src/__tests__/ReactFlightTurbopackDOMBrowser-test.js
index a62ce7b8e74e0..d9061d8e44231 100644
--- a/packages/react-server-dom-turbopack/src/__tests__/ReactFlightTurbopackDOMBrowser-test.js
+++ b/packages/react-server-dom-turbopack/src/__tests__/ReactFlightTurbopackDOMBrowser-test.js
@@ -19,10 +19,12 @@ global.WritableStream =
 global.TextEncoder = require('util').TextEncoder;
 global.TextDecoder = require('util').TextDecoder;
 
+let clientExports;
 let React;
 let ReactDOMClient;
 let ReactServerDOMServer;
 let ReactServerDOMClient;
+let ReactServer;
 let ReactServerScheduler;
 let act;
 let serverAct;
@@ -39,10 +41,13 @@ describe('ReactFlightTurbopackDOMBrowser', () => {
 
     // Simulate the condition resolution
     jest.mock('react', () => require('react/react.react-server'));
+    ReactServer = require('react');
+
     jest.mock('react-server-dom-turbopack/server', () =>
       require('react-server-dom-turbopack/server.browser'),
     );
     const TurbopackMock = require('./utils/TurbopackMock');
+    clientExports = TurbopackMock.clientExports;
     turbopackMap = TurbopackMock.turbopackMap;
 
     ReactServerDOMServer = require('react-server-dom-turbopack/server.browser');
@@ -77,6 +82,15 @@ describe('ReactFlightTurbopackDOMBrowser', () => {
     });
   }
 
+  function normalizeCodeLocInfo(str) {
+    return (
+      str &&
+      str.replace(/^ +(?:at|in) ([\S]+)[^\n]*/gm, function (m, name) {
+        return '    in ' + name + (/\d/.test(m) ? ' (at **)' : '');
+      })
+    );
+  }
+
   it('should resolve HTML using W3C streams', async () => {
     function Text({children}) {
       return <span>{children}</span>;
@@ -163,4 +177,74 @@ describe('ReactFlightTurbopackDOMBrowser', () => {
 
     expect(container.innerHTML).toBe('<div>Hi</div>');
   });
+
+  it('can transport debug info through a dedicated debug channel', async () => {
+    let ownerStack;
+
+    const ClientComponent = clientExports(() => {
+      ownerStack = React.captureOwnerStack ? React.captureOwnerStack() : null;
+      return <p>Hi</p>;
+    });
+
+    function App() {
+      return ReactServer.createElement(
+        ReactServer.Suspense,
+        null,
+        ReactServer.createElement(ClientComponent, null),
+      );
+    }
+
+    let debugReadableStreamController;
+
+    const debugReadableStream = new ReadableStream({
+      start(controller) {
+        debugReadableStreamController = controller;
+      },
+    });
+
+    const rscStream = await serverAct(() =>
+      ReactServerDOMServer.renderToReadableStream(
+        ReactServer.createElement(App, null),
+        turbopackMap,
+        {
+          debugChannel: {
+            writable: new WritableStream({
+              write(chunk) {
+                debugReadableStreamController.enqueue(chunk);
+              },
+              close() {
+                debugReadableStreamController.close();
+              },
+            }),
+          },
+        },
+      ),
+    );
+
+    function ClientRoot({response}) {
+      return use(response);
+    }
+
+    const response = ReactServerDOMClient.createFromReadableStream(rscStream, {
+      replayConsoleLogs: true,
+      debugChannel: {
+        readable: debugReadableStream,
+        // Explicitly not defining a writable side here. Its presence was
+        // previously used as a condition to wait for referenced debug chunks.
+      },
+    });
+
+    const container = document.createElement('div');
+    const root = ReactDOMClient.createRoot(container);
+
+    await act(() => {
+      root.render(<ClientRoot response={response} />);
+    });
+
+    if (__DEV__) {
+      expect(normalizeCodeLocInfo(ownerStack)).toBe('\n    in App (at **)');
+    }
+
+    expect(container.innerHTML).toBe('<p>Hi</p>');
+  });
 });
diff --git a/packages/react-server-dom-turbopack/src/__tests__/ReactFlightTurbopackDOMEdge-test.js b/packages/react-server-dom-turbopack/src/__tests__/ReactFlightTurbopackDOMEdge-test.js
index be3e7e476d91f..ec2d42201b97a 100644
--- a/packages/react-server-dom-turbopack/src/__tests__/ReactFlightTurbopackDOMEdge-test.js
+++ b/packages/react-server-dom-turbopack/src/__tests__/ReactFlightTurbopackDOMEdge-test.js
@@ -241,4 +241,101 @@ describe('ReactFlightTurbopackDOMEdge', () => {
       'Switched to client rendering because the server rendering errored:\n\nssr-throw',
     );
   });
+
+  // @gate __DEV__
+  it('can transport debug info through a slow debug channel', async () => {
+    function Thrower() {
+      throw new Error('ssr-throw');
+    }
+
+    const ClientComponentOnTheClient = clientExports(
+      Thrower,
+      123,
+      'path/to/chunk.js',
+    );
+
+    const ClientComponentOnTheServer = clientExports(Thrower);
+
+    function App() {
+      return ReactServer.createElement(
+        ReactServer.Suspense,
+        null,
+        ReactServer.createElement(ClientComponentOnTheClient, null),
+      );
+    }
+
+    let debugReadableStreamController;
+
+    const debugReadableStream = new ReadableStream({
+      start(controller) {
+        debugReadableStreamController = controller;
+      },
+    });
+
+    const rscStream = await serverAct(() =>
+      ReactServerDOMServer.renderToReadableStream(
+        ReactServer.createElement(App, null),
+        turbopackMap,
+        {
+          debugChannel: {
+            writable: new WritableStream({
+              write(chunk) {
+                debugReadableStreamController.enqueue(chunk);
+              },
+              close() {
+                debugReadableStreamController.close();
+              },
+            }),
+          },
+        },
+      ),
+    );
+
+    function ClientRoot({response}) {
+      return use(response);
+    }
+
+    const serverConsumerManifest = {
+      moduleMap: {
+        [turbopackMap[ClientComponentOnTheClient.$$id].id]: {
+          '*': turbopackMap[ClientComponentOnTheServer.$$id],
+        },
+      },
+      moduleLoading: null,
+    };
+
+    const response = ReactServerDOMClient.createFromReadableStream(rscStream, {
+      serverConsumerManifest,
+      debugChannel: {
+        readable:
+          // Create a delayed stream to simulate that the debug stream might
+          // be transported slower than the RSC stream, which must not lead to
+          // missing debug info.
+          createDelayedStream(debugReadableStream),
+      },
+    });
+
+    let ownerStack;
+
+    const ssrStream = await serverAct(() =>
+      ReactDOMServer.renderToReadableStream(
+        <ClientRoot response={response} />,
+        {
+          onError(err, errorInfo) {
+            ownerStack = React.captureOwnerStack
+              ? React.captureOwnerStack()
+              : null;
+          },
+        },
+      ),
+    );
+
+    const result = await readResult(ssrStream);
+
+    expect(normalizeCodeLocInfo(ownerStack)).toBe('\n    in App (at **)');
+
+    expect(result).toContain(
+      'Switched to client rendering because the server rendering errored:\n\nssr-throw',
+    );
+  });
 });
diff --git a/packages/react-server-dom-turbopack/src/__tests__/ReactFlightTurbopackDOMNode-test.js b/packages/react-server-dom-turbopack/src/__tests__/ReactFlightTurbopackDOMNode-test.js
index 1fcf52fde4443..59e8ea3947094 100644
--- a/packages/react-server-dom-turbopack/src/__tests__/ReactFlightTurbopackDOMNode-test.js
+++ b/packages/react-server-dom-turbopack/src/__tests__/ReactFlightTurbopackDOMNode-test.js
@@ -91,15 +91,19 @@ describe('ReactFlightTurbopackDOMNode', () => {
   }
 
   function createDelayedStream() {
-    return new Stream.Transform({
+    let resolveDelayedStream;
+    const promise = new Promise(resolve => (resolveDelayedStream = resolve));
+    const delayedStream = new Stream.Transform({
       ...streamOptions,
       transform(chunk, encoding, callback) {
-        setTimeout(() => {
+        // Artificially delay pushing the chunk.
+        promise.then(() => {
           this.push(chunk);
           callback();
         });
       },
     });
+    return {delayedStream, resolveDelayedStream};
   }
 
   it('should allow an alternative module mapping to be used for SSR', async () => {
@@ -202,8 +206,102 @@ describe('ReactFlightTurbopackDOMNode', () => {
 
     // Create a delayed stream to simulate that the RSC stream might be
     // transported slower than the debug channel, which must not lead to a
-    // `controller.enqueueModel is not a function` error in the Flight client.
-    const readable = createDelayedStream();
+    // `Connection closed` error in the Flight client.
+    const {delayedStream, resolveDelayedStream} = createDelayedStream();
+
+    rscStream.pipe(delayedStream);
+
+    function ClientRoot({response}) {
+      return use(response);
+    }
+
+    const serverConsumerManifest = {
+      moduleMap: {
+        [turbopackMap[ClientComponentOnTheClient.$$id].id]: {
+          '*': turbopackMap[ClientComponentOnTheServer.$$id],
+        },
+      },
+      moduleLoading: null,
+    };
+
+    const response = ReactServerDOMClient.createFromNodeStream(
+      delayedStream,
+      serverConsumerManifest,
+      {debugChannel: debugReadable},
+    );
+
+    setTimeout(resolveDelayedStream);
+
+    let ownerStack;
+
+    const ssrStream = await serverAct(() =>
+      ReactDOMServer.renderToPipeableStream(
+        <ClientRoot response={response} />,
+        {
+          onError(err, errorInfo) {
+            ownerStack = React.captureOwnerStack
+              ? React.captureOwnerStack()
+              : null;
+          },
+        },
+      ),
+    );
+
+    const result = await readResult(ssrStream);
+
+    expect(normalizeCodeLocInfo(ownerStack)).toBe('\n    in App (at **)');
+
+    expect(result).toContain(
+      'Switched to client rendering because the server rendering errored:\n\nssr-throw',
+    );
+  });
+
+  // @gate __DEV__
+  it('can transport debug info through a slow debug channel', async () => {
+    function Thrower() {
+      throw new Error('ssr-throw');
+    }
+
+    const ClientComponentOnTheClient = clientExports(
+      Thrower,
+      123,
+      'path/to/chunk.js',
+    );
+
+    const ClientComponentOnTheServer = clientExports(Thrower);
+
+    function App() {
+      return ReactServer.createElement(
+        ReactServer.Suspense,
+        null,
+        ReactServer.createElement(ClientComponentOnTheClient, null),
+      );
+    }
+
+    // Create a delayed stream to simulate that the debug stream might be
+    // transported slower than the RSC stream, which must not lead to missing
+    // debug info.
+    const {delayedStream, resolveDelayedStream} = createDelayedStream();
+
+    const rscStream = await serverAct(() =>
+      ReactServerDOMServer.renderToPipeableStream(
+        ReactServer.createElement(App, null),
+        turbopackMap,
+        {
+          debugChannel: new Stream.Writable({
+            write(chunk, encoding, callback) {
+              delayedStream.write(chunk, encoding);
+              callback();
+            },
+            final() {
+              delayedStream.end();
+            },
+          }),
+        },
+      ),
+    );
+
+    const readable = new Stream.PassThrough(streamOptions);
 
     rscStream.pipe(readable);
 
@@ -223,9 +321,11 @@ describe('ReactFlightTurbopackDOMNode', () => {
     const response = ReactServerDOMClient.createFromNodeStream(
       readable,
       serverConsumerManifest,
-      {debugChannel: debugReadable},
+      {debugChannel: delayedStream},
     );
 
+    setTimeout(resolveDelayedStream);
+
     let ownerStack;
 
     const ssrStream = await serverAct(() =>
diff --git a/packages/react-server-dom-turbopack/src/client/ReactFlightDOMClientBrowser.js b/packages/react-server-dom-turbopack/src/client/ReactFlightDOMClientBrowser.js
index 1ca44135a4b8c..dc4c99dabd055 100644
--- a/packages/react-server-dom-turbopack/src/client/ReactFlightDOMClientBrowser.js
+++ b/packages/react-server-dom-turbopack/src/client/ReactFlightDOMClientBrowser.js
@@ -10,9 +10,10 @@
 import type {Thenable} from 'shared/ReactTypes.js';
 
 import type {
-  Response as FlightResponse,
-  FindSourceMapURLCallback,
+  DebugChannel,
   DebugChannelCallback,
+  FindSourceMapURLCallback,
+  Response as FlightResponse,
 } from 'react-client/src/ReactFlightClient';
 
 import type {ReactServerValue} from 'react-client/src/ReactFlightReplyClient';
@@ -71,6 +72,19 @@ function createDebugCallbackFromWritableStream(
 }
 
 function createResponseFromOptions(options: void | Options) {
+  const debugChannel: void | DebugChannel =
+    __DEV__ && options && options.debugChannel !== undefined
+      ? {
+          hasReadable: options.debugChannel.readable !== undefined,
+          callback:
+            options.debugChannel.writable !== undefined
+              ? createDebugCallbackFromWritableStream(
+                  options.debugChannel.writable,
+                )
+              : null,
+        }
+      : undefined;
+
   return createResponse(
     null,
     null,
@@ -88,12 +102,7 @@ function createResponseFromOptions(options: void | Options) {
     __DEV__ && options && options.environmentName
       ? options.environmentName
       : undefined,
-    __DEV__ &&
-      options &&
-      options.debugChannel !== undefined &&
-      options.debugChannel.writable !== undefined
-      ? createDebugCallbackFromWritableStream(options.debugChannel.writable)
-      : undefined,
+    debugChannel,
   );
 }
 
diff --git a/packages/react-server-dom-turbopack/src/client/ReactFlightDOMClientEdge.js b/packages/react-server-dom-turbopack/src/client/ReactFlightDOMClientEdge.js
index 4c7e99d2149bc..245761b2722a6 100644
--- a/packages/react-server-dom-turbopack/src/client/ReactFlightDOMClientEdge.js
+++ b/packages/react-server-dom-turbopack/src/client/ReactFlightDOMClientEdge.js
@@ -10,6 +10,7 @@
 import type {Thenable, ReactCustomFormAction} from 'shared/ReactTypes.js';
 
 import type {
+  DebugChannel,
   Response as FlightResponse,
   FindSourceMapURLCallback,
 } from 'react-client/src/ReactFlightClient';
@@ -83,6 +84,14 @@ export type Options = {
 };
 
 function createResponseFromOptions(options: Options) {
+  const debugChannel: void | DebugChannel =
+    __DEV__ && options && options.debugChannel !== undefined
+      ? {
+          hasReadable: options.debugChannel.readable !== undefined,
+          callback: null,
+        }
+      : undefined;
+
   return createResponse(
     options.serverConsumerManifest.moduleMap,
     options.serverConsumerManifest.serverModuleMap,
@@ -100,6 +109,7 @@ function createResponseFromOptions(options: Options) {
     __DEV__ && options && options.environmentName
       ? options.environmentName
       : undefined,
+    debugChannel,
   );
 }
 
diff --git a/packages/react-server-dom-turbopack/src/client/ReactFlightDOMClientNode.js b/packages/react-server-dom-turbopack/src/client/ReactFlightDOMClientNode.js
index 97e9be1bcddf6..af8b7f41bc837 100644
--- a/packages/react-server-dom-turbopack/src/client/ReactFlightDOMClientNode.js
+++ b/packages/react-server-dom-turbopack/src/client/ReactFlightDOMClientNode.js
@@ -10,8 +10,9 @@
 import type {Thenable, ReactCustomFormAction} from 'shared/ReactTypes.js';
 
 import type {
-  Response,
+  DebugChannel,
   FindSourceMapURLCallback,
+  Response,
 } from 'react-client/src/ReactFlightClient';
 
 import type {
@@ -90,6 +91,14 @@ function createFromNodeStream<T>(
   serverConsumerManifest: ServerConsumerManifest,
   options?: Options,
 ): Thenable<T> {
+  const debugChannel: void | DebugChannel =
+    __DEV__ && options && options.debugChannel !== undefined
+      ? {
+          hasReadable: options.debugChannel.readable !== undefined,
+          callback: null,
+        }
+      : undefined;
+
   const response: Response = createResponse(
     serverConsumerManifest.moduleMap,
     serverConsumerManifest.serverModuleMap,
@@ -105,6 +114,7 @@ function createFromNodeStream<T>(
     __DEV__ && options && options.environmentName
       ? options.environmentName
       : undefined,
+    debugChannel,
   );
 
   if (__DEV__ && options && options.debugChannel) {
diff --git a/packages/react-server-dom-webpack/src/__tests__/ReactFlightDOMBrowser-test.js b/packages/react-server-dom-webpack/src/__tests__/ReactFlightDOMBrowser-test.js
index 969bd493f3f47..cd546f61359dc 100644
--- a/packages/react-server-dom-webpack/src/__tests__/ReactFlightDOMBrowser-test.js
+++ b/packages/react-server-dom-webpack/src/__tests__/ReactFlightDOMBrowser-test.js
@@ -174,6 +174,15 @@ describe('ReactFlightDOMBrowser', () => {
     });
   }
 
+  function normalizeCodeLocInfo(str) {
+    return (
+      str &&
+      str.replace(/^ +(?:at|in) ([\S]+)[^\n]*/gm, function (m, name) {
+        return '    in ' + name + (/\d/.test(m) ? ' (at **)' : '');
+      })
+    );
+  }
+
   it('should resolve HTML using W3C streams', async () => {
     function Text({children}) {
       return <span>{children}</span>;
@@ -2767,4 +2776,74 @@ describe('ReactFlightDOMBrowser', () => {
 
     expect(container.innerHTML).toBe('<div>Hi</div>');
   });
+
+  it('can transport debug info through a dedicated debug channel', async () => {
+    let ownerStack;
+
+    const ClientComponent = clientExports(() => {
+      ownerStack = React.captureOwnerStack ? React.captureOwnerStack() : null;
+      return <p>Hi</p>;
+    });
+
+    function App() {
+      return ReactServer.createElement(
+        ReactServer.Suspense,
+        null,
+        ReactServer.createElement(ClientComponent, null),
+      );
+    }
+
+    let debugReadableStreamController;
+
+    const debugReadableStream = new ReadableStream({
+      start(controller) {
+        debugReadableStreamController = controller;
+      },
+    });
+
+    const rscStream = await serverAct(() =>
+      ReactServerDOMServer.renderToReadableStream(
+        ReactServer.createElement(App, null),
+        webpackMap,
+        {
+          debugChannel: {
+            writable: new WritableStream({
+              write(chunk) {
+                debugReadableStreamController.enqueue(chunk);
+              },
+              close() {
+                debugReadableStreamController.close();
+              },
+            }),
+          },
+        },
+      ),
+    );
+
+    function ClientRoot({response}) {
+      return use(response);
+    }
+
+    const response = ReactServerDOMClient.createFromReadableStream(rscStream, {
+      replayConsoleLogs: true,
+      debugChannel: {
+        readable: debugReadableStream,
+        // Explicitly not defining a writable side here. Its presence was
+        // previously used as a condition to wait for referenced debug chunks.
+      },
+    });
+
+    const container = document.createElement('div');
+    const root = ReactDOMClient.createRoot(container);
+
+    await act(() => {
+      root.render(<ClientRoot response={response} />);
+    });
+
+    if (__DEV__) {
+      expect(normalizeCodeLocInfo(ownerStack)).toBe('\n    in App (at **)');
+    }
+
+    expect(container.innerHTML).toBe('<p>Hi</p>');
+  });
 });
diff --git a/packages/react-server-dom-webpack/src/__tests__/ReactFlightDOMEdge-test.js b/packages/react-server-dom-webpack/src/__tests__/ReactFlightDOMEdge-test.js
index bd93cc575653e..98bc21576b08a 100644
--- a/packages/react-server-dom-webpack/src/__tests__/ReactFlightDOMEdge-test.js
+++ b/packages/react-server-dom-webpack/src/__tests__/ReactFlightDOMEdge-test.js
@@ -2089,4 +2089,103 @@ describe('ReactFlightDOMEdge', () => {
       'Switched to client rendering because the server rendering errored:\n\nssr-throw',
     );
   });
+
+  // @gate __DEV__
+  it('can transport debug info through a slow debug channel', async () => {
+    function Thrower() {
+      throw new Error('ssr-throw');
+    }
+
+    const ClientComponentOnTheClient = clientExports(
+      Thrower,
+      123,
+      'path/to/chunk.js',
+    );
+
+    const ClientComponentOnTheServer = clientExports(Thrower);
+
+    function App() {
+      return ReactServer.createElement(
+        ReactServer.Suspense,
+        null,
+        ReactServer.createElement(ClientComponentOnTheClient, null),
+      );
+    }
+
+    let debugReadableStreamController;
+
+    const debugReadableStream = new ReadableStream({
+      start(controller) {
+        debugReadableStreamController = controller;
+      },
+    });
+
+    const rscStream = await serverAct(() =>
+      passThrough(
+        ReactServerDOMServer.renderToReadableStream(
+          ReactServer.createElement(App, null),
+          webpackMap,
+          {
+            debugChannel: {
+              writable: new WritableStream({
+                write(chunk) {
+                  debugReadableStreamController.enqueue(chunk);
+                },
+                close() {
+                  debugReadableStreamController.close();
+                },
+              }),
+            },
+          },
+        ),
+      ),
+    );
+
+    function ClientRoot({response}) {
+      return use(response);
+    }
+
+    const serverConsumerManifest = {
+      moduleMap: {
+        [webpackMap[ClientComponentOnTheClient.$$id].id]: {
+          '*': webpackMap[ClientComponentOnTheServer.$$id],
+        },
+      },
+      moduleLoading: webpackModuleLoading,
+    };
+
+    const response = ReactServerDOMClient.createFromReadableStream(rscStream, {
+      serverConsumerManifest,
+      debugChannel: {
+        readable:
+          // Create a delayed stream to simulate that the debug stream might be
+          // transported slower than the RSC stream, which must not lead to
+          // missing debug info.
+          createDelayedStream(debugReadableStream),
+      },
+    });
+
+    let ownerStack;
+
+    const ssrStream = await serverAct(() =>
+      ReactDOMServer.renderToReadableStream(
+        <ClientRoot response={response} />,
+        {
+          onError(err, errorInfo) {
+            ownerStack = React.captureOwnerStack
+              ? React.captureOwnerStack()
+              : null;
+          },
+        },
+      ),
+    );
+
+    const result = await readResult(ssrStream);
+
+    expect(normalizeCodeLocInfo(ownerStack)).toBe('\n    in App (at **)');
+
+    expect(result).toContain(
+      'Switched to client rendering because the server rendering errored:\n\nssr-throw',
+    );
+  });
 });
diff --git a/packages/react-server-dom-webpack/src/__tests__/ReactFlightDOMNode-test.js b/packages/react-server-dom-webpack/src/__tests__/ReactFlightDOMNode-test.js
index 2ee9bfa961c2b..f069b23b293c0 100644
--- a/packages/react-server-dom-webpack/src/__tests__/ReactFlightDOMNode-test.js
+++ b/packages/react-server-dom-webpack/src/__tests__/ReactFlightDOMNode-test.js
@@ -152,16 +152,19 @@ describe('ReactFlightDOMNode', () => {
   }
 
   function createDelayedStream() {
-    return new Stream.Transform({
+    let resolveDelayedStream;
+    const promise = new Promise(resolve => (resolveDelayedStream = resolve));
+    const delayedStream = new Stream.Transform({
       ...streamOptions,
       transform(chunk, encoding, callback) {
-        // Artificially delay between pushing chunks.
-        setTimeout(() => {
+        // Artificially delay pushing the chunk.
+        promise.then(() => {
           this.push(chunk);
           callback();
         });
       },
     });
+    return {delayedStream, resolveDelayedStream};
   }
 
   it('should support web streams in node', async () => {
@@ -963,8 +966,102 @@ describe('ReactFlightDOMNode', () => {
 
     // Create a delayed stream to simulate that the RSC stream might be
     // transported slower than the debug channel, which must not lead to a
-    // `controller.enqueueModel is not a function` error in the Flight client.
-    const readable = createDelayedStream();
+    // `Connection closed` error in the Flight client.
+    const {delayedStream, resolveDelayedStream} = createDelayedStream();
+
+    rscStream.pipe(delayedStream);
+
+    function ClientRoot({response}) {
+      return use(response);
+    }
+
+    const serverConsumerManifest = {
+      moduleMap: {
+        [webpackMap[ClientComponentOnTheClient.$$id].id]: {
+          '*': webpackMap[ClientComponentOnTheServer.$$id],
+        },
+      },
+      moduleLoading: webpackModuleLoading,
+    };
+
+    const response = ReactServerDOMClient.createFromNodeStream(
+      delayedStream,
+      serverConsumerManifest,
+      {debugChannel: debugReadable},
+    );
+
+    setTimeout(resolveDelayedStream);
+
+    let ownerStack;
+
+    const ssrStream = await serverAct(() =>
+      ReactDOMServer.renderToPipeableStream(
+        <ClientRoot response={response} />,
+        {
+          onError(err, errorInfo) {
+            ownerStack = React.captureOwnerStack
+              ? React.captureOwnerStack()
+              : null;
+          },
+        },
+      ),
+    );
+
+    const result = await readResult(ssrStream);
+
+    expect(normalizeCodeLocInfo(ownerStack)).toBe('\n    in App (at **)');
+
+    expect(result).toContain(
+      'Switched to client rendering because the server rendering errored:\n\nssr-throw',
+    );
+  });
+
+  // @gate __DEV__
+  it('can transport debug info through a slow debug channel', async () => {
+    function Thrower() {
+      throw new Error('ssr-throw');
+    }
+
+    const ClientComponentOnTheClient = clientExports(
+      Thrower,
+      123,
+      'path/to/chunk.js',
+    );
+
+    const ClientComponentOnTheServer = clientExports(Thrower);
+
+    function App() {
+      return ReactServer.createElement(
+        ReactServer.Suspense,
+        null,
+        ReactServer.createElement(ClientComponentOnTheClient, null),
+      );
+    }
+
+    // Create a delayed stream to simulate that the debug stream might be
+    // transported slower than the RSC stream, which must not lead to missing
+    // debug info.
+    const {delayedStream, resolveDelayedStream} = createDelayedStream();
+
+    const rscStream = await serverAct(() =>
+      ReactServerDOMServer.renderToPipeableStream(
+        ReactServer.createElement(App, null),
+        webpackMap,
+        {
+          debugChannel: new Stream.Writable({
+            write(chunk, encoding, callback) {
+              delayedStream.write(chunk, encoding);
+              callback();
+            },
+            final() {
+              delayedStream.end();
+            },
+          }),
+        },
+      ),
+    );
+
+    const readable = new Stream.PassThrough(streamOptions);
 
     rscStream.pipe(readable);
 
@@ -984,9 +1081,11 @@ describe('ReactFlightDOMNode', () => {
     const response = ReactServerDOMClient.createFromNodeStream(
       readable,
       serverConsumerManifest,
-      {debugChannel: debugReadable},
+      {debugChannel: delayedStream},
     );
 
+    setTimeout(resolveDelayedStream);
+
     let ownerStack;
 
     const ssrStream = await serverAct(() =>
diff --git a/packages/react-server-dom-webpack/src/client/ReactFlightDOMClientBrowser.js b/packages/react-server-dom-webpack/src/client/ReactFlightDOMClientBrowser.js
index 1ca44135a4b8c..dc4c99dabd055 100644
--- a/packages/react-server-dom-webpack/src/client/ReactFlightDOMClientBrowser.js
+++ b/packages/react-server-dom-webpack/src/client/ReactFlightDOMClientBrowser.js
@@ -10,9 +10,10 @@
 import type {Thenable} from 'shared/ReactTypes.js';
 
 import type {
-  Response as FlightResponse,
-  FindSourceMapURLCallback,
+  DebugChannel,
   DebugChannelCallback,
+  FindSourceMapURLCallback,
+  Response as FlightResponse,
 } from 'react-client/src/ReactFlightClient';
 
 import type {ReactServerValue} from 'react-client/src/ReactFlightReplyClient';
@@ -71,6 +72,19 @@ function createDebugCallbackFromWritableStream(
 }
 
 function createResponseFromOptions(options: void | Options) {
+  const debugChannel: void | DebugChannel =
+    __DEV__ && options && options.debugChannel !== undefined
+      ? {
+          hasReadable: options.debugChannel.readable !== undefined,
+          callback:
+            options.debugChannel.writable !== undefined
+              ? createDebugCallbackFromWritableStream(
+                  options.debugChannel.writable,
+                )
+              : null,
+        }
+      : undefined;
+
   return createResponse(
     null,
     null,
@@ -88,12 +102,7 @@ function createResponseFromOptions(options: void | Options) {
     __DEV__ && options && options.environmentName
       ? options.environmentName
       : undefined,
-    __DEV__ &&
-      options &&
-      options.debugChannel !== undefined &&
-      options.debugChannel.writable !== undefined
-      ? createDebugCallbackFromWritableStream(options.debugChannel.writable)
-      : undefined,
+    debugChannel,
   );
 }
 
diff --git a/packages/react-server-dom-webpack/src/client/ReactFlightDOMClientEdge.js b/packages/react-server-dom-webpack/src/client/ReactFlightDOMClientEdge.js
index 4c7e99d2149bc..7c9a707a546a6 100644
--- a/packages/react-server-dom-webpack/src/client/ReactFlightDOMClientEdge.js
+++ b/packages/react-server-dom-webpack/src/client/ReactFlightDOMClientEdge.js
@@ -10,8 +10,9 @@
 import type {Thenable, ReactCustomFormAction} from 'shared/ReactTypes.js';
 
 import type {
-  Response as FlightResponse,
+  DebugChannel,
   FindSourceMapURLCallback,
+  Response as FlightResponse,
 } from 'react-client/src/ReactFlightClient';
 
 import type {ReactServerValue} from 'react-client/src/ReactFlightReplyClient';
@@ -83,6 +84,14 @@ export type Options = {
 };
 
 function createResponseFromOptions(options: Options) {
+  const debugChannel: void | DebugChannel =
+    __DEV__ && options && options.debugChannel !== undefined
+      ? {
+          hasReadable: options.debugChannel.readable !== undefined,
+          callback: null,
+        }
+      : undefined;
+
   return createResponse(
     options.serverConsumerManifest.moduleMap,
     options.serverConsumerManifest.serverModuleMap,
@@ -100,6 +109,7 @@ function createResponseFromOptions(options: Options) {
     __DEV__ && options && options.environmentName
       ? options.environmentName
       : undefined,
+    debugChannel,
   );
 }
 
diff --git a/packages/react-server-dom-webpack/src/client/ReactFlightDOMClientNode.js b/packages/react-server-dom-webpack/src/client/ReactFlightDOMClientNode.js
index 97e9be1bcddf6..af8b7f41bc837 100644
--- a/packages/react-server-dom-webpack/src/client/ReactFlightDOMClientNode.js
+++ b/packages/react-server-dom-webpack/src/client/ReactFlightDOMClientNode.js
@@ -10,8 +10,9 @@
 import type {Thenable, ReactCustomFormAction} from 'shared/ReactTypes.js';
 
 import type {
-  Response,
+  DebugChannel,
   FindSourceMapURLCallback,
+  Response,
 } from 'react-client/src/ReactFlightClient';
 
 import type {
@@ -90,6 +91,14 @@ function createFromNodeStream<T>(
   serverConsumerManifest: ServerConsumerManifest,
   options?: Options,
 ): Thenable<T> {
+  const debugChannel: void | DebugChannel =
+    __DEV__ && options && options.debugChannel !== undefined
+      ? {
+          hasReadable: options.debugChannel.readable !== undefined,
+          callback: null,
+        }
+      : undefined;
+
   const response: Response = createResponse(
     serverConsumerManifest.moduleMap,
     serverConsumerManifest.serverModuleMap,
@@ -105,6 +114,7 @@ function createFromNodeStream<T>(
     __DEV__ && options && options.environmentName
       ? options.environmentName
       : undefined,
+    debugChannel,
   );
 
   if (__DEV__ && options && options.debugChannel) {