diff --git a/packages/snaps-controllers/coverage.json b/packages/snaps-controllers/coverage.json
index 993ff36acf..b8cc8451e6 100644
--- a/packages/snaps-controllers/coverage.json
+++ b/packages/snaps-controllers/coverage.json
@@ -1,6 +1,6 @@
 {
-  "branches": 93.61,
+  "branches": 93.64,
   "functions": 98.16,
   "lines": 98.5,
-  "statements": 98.33
+  "statements": 98.34
 }
diff --git a/packages/snaps-controllers/src/snaps/SnapController.test.tsx b/packages/snaps-controllers/src/snaps/SnapController.test.tsx
index 2c33a87d89..84a2117975 100644
--- a/packages/snaps-controllers/src/snaps/SnapController.test.tsx
+++ b/packages/snaps-controllers/src/snaps/SnapController.test.tsx
@@ -77,6 +77,7 @@ import { inc } from 'semver';
 
 import {
   LEGACY_ENCRYPTION_KEY_DERIVATION_OPTIONS,
+  METAMASK_ORIGIN,
   STATE_DEBOUNCE_TIMEOUT,
 } from './constants';
 import { SnapsRegistryStatus } from './registry';
@@ -2243,7 +2244,7 @@ describe('SnapController', () => {
       expect(
         await snapController.handleRequest({
           snapId: snap.id,
-          origin: MOCK_ORIGIN,
+          origin: METAMASK_ORIGIN,
           handler: HandlerType.OnUserInput,
           request: {
             jsonrpc: '2.0',
@@ -2294,7 +2295,7 @@ describe('SnapController', () => {
       expect(
         await snapController.handleRequest({
           snapId: snap.id,
-          origin: 'metamask',
+          origin: METAMASK_ORIGIN,
           handler: HandlerType.OnRpcRequest,
           request: { jsonrpc: '2.0', method: 'test' },
         }),
@@ -2341,7 +2342,7 @@ describe('SnapController', () => {
       expect(
         await snapController.handleRequest({
           snapId: snap.id,
-          origin: 'metamask',
+          origin: METAMASK_ORIGIN,
           handler: HandlerType.OnKeyringRequest,
           request: { jsonrpc: '2.0', method: 'test' },
         }),
@@ -2807,7 +2808,7 @@ describe('SnapController', () => {
 
       await snapController.handleRequest({
         snapId: MOCK_SNAP_ID,
-        origin: MOCK_ORIGIN,
+        origin: METAMASK_ORIGIN,
         handler: HandlerType.OnUserInput,
         request: {
           jsonrpc: '2.0',
@@ -2827,7 +2828,7 @@ describe('SnapController', () => {
         'ExecutionService:handleRpcRequest',
         MOCK_SNAP_ID,
         {
-          origin: MOCK_ORIGIN,
+          origin: METAMASK_ORIGIN,
           handler: HandlerType.OnUserInput,
           request: {
             id: expect.any(String),
@@ -2896,7 +2897,7 @@ describe('SnapController', () => {
       await expect(
         snapController.handleRequest({
           snapId: MOCK_SNAP_ID,
-          origin: MOCK_ORIGIN,
+          origin: METAMASK_ORIGIN,
           handler: HandlerType.OnTransaction,
           request: {
             jsonrpc: '2.0',
@@ -2952,7 +2953,7 @@ describe('SnapController', () => {
       await expect(
         snapController.handleRequest({
           snapId: MOCK_SNAP_ID,
-          origin: MOCK_ORIGIN,
+          origin: METAMASK_ORIGIN,
           handler: HandlerType.OnTransaction,
           request: {
             jsonrpc: '2.0',
@@ -3007,7 +3008,7 @@ describe('SnapController', () => {
 
       const result = await snapController.handleRequest({
         snapId: MOCK_SNAP_ID,
-        origin: MOCK_ORIGIN,
+        origin: METAMASK_ORIGIN,
         handler: HandlerType.OnTransaction,
         request: {
           jsonrpc: '2.0',
@@ -3062,7 +3063,7 @@ describe('SnapController', () => {
       await expect(
         snapController.handleRequest({
           snapId: MOCK_SNAP_ID,
-          origin: MOCK_ORIGIN,
+          origin: METAMASK_ORIGIN,
           handler: HandlerType.OnTransaction,
           request: {
             jsonrpc: '2.0',
@@ -3120,7 +3121,7 @@ describe('SnapController', () => {
 
       const result = await snapController.handleRequest({
         snapId: MOCK_SNAP_ID,
-        origin: MOCK_ORIGIN,
+        origin: METAMASK_ORIGIN,
         handler: HandlerType.OnTransaction,
         request: {
           jsonrpc: '2.0',
@@ -3183,7 +3184,7 @@ describe('SnapController', () => {
       await expect(
         snapController.handleRequest({
           snapId: MOCK_SNAP_ID,
-          origin: MOCK_ORIGIN,
+          origin: METAMASK_ORIGIN,
           handler: HandlerType.OnSignature,
           request: {
             jsonrpc: '2.0',
@@ -3239,7 +3240,7 @@ describe('SnapController', () => {
       await expect(
         snapController.handleRequest({
           snapId: MOCK_SNAP_ID,
-          origin: MOCK_ORIGIN,
+          origin: METAMASK_ORIGIN,
           handler: HandlerType.OnSignature,
           request: {
             jsonrpc: '2.0',
@@ -3295,7 +3296,7 @@ describe('SnapController', () => {
       await expect(
         snapController.handleRequest({
           snapId: MOCK_SNAP_ID,
-          origin: MOCK_ORIGIN,
+          origin: METAMASK_ORIGIN,
           handler: HandlerType.OnSignature,
           request: {
             jsonrpc: '2.0',
@@ -3348,7 +3349,7 @@ describe('SnapController', () => {
 
       const result = await snapController.handleRequest({
         snapId: MOCK_SNAP_ID,
-        origin: MOCK_ORIGIN,
+        origin: METAMASK_ORIGIN,
         handler: HandlerType.OnSignature,
         request: {
           jsonrpc: '2.0',
@@ -3402,7 +3403,7 @@ describe('SnapController', () => {
     expect(
       await snapController.handleRequest({
         snapId: MOCK_SNAP_ID,
-        origin: MOCK_ORIGIN,
+        origin: METAMASK_ORIGIN,
         handler: HandlerType.OnTransaction,
         request: {
           jsonrpc: '2.0',
@@ -3454,7 +3455,7 @@ describe('SnapController', () => {
     expect(
       await snapController.handleRequest({
         snapId: MOCK_SNAP_ID,
-        origin: MOCK_ORIGIN,
+        origin: METAMASK_ORIGIN,
         handler: HandlerType.OnSignature,
         request: {
           jsonrpc: '2.0',
@@ -3516,7 +3517,7 @@ describe('SnapController', () => {
     await expect(
       snapController.handleRequest({
         snapId: MOCK_SNAP_ID,
-        origin: MOCK_ORIGIN,
+        origin: METAMASK_ORIGIN,
         handler: HandlerType.OnHomePage,
         request: {
           jsonrpc: '2.0',
@@ -3570,7 +3571,7 @@ describe('SnapController', () => {
     await expect(
       snapController.handleRequest({
         snapId: MOCK_SNAP_ID,
-        origin: MOCK_ORIGIN,
+        origin: METAMASK_ORIGIN,
         handler: HandlerType.OnHomePage,
         request: {
           jsonrpc: '2.0',
@@ -3623,7 +3624,7 @@ describe('SnapController', () => {
 
     const result = await snapController.handleRequest({
       snapId: MOCK_SNAP_ID,
-      origin: MOCK_ORIGIN,
+      origin: METAMASK_ORIGIN,
       handler: HandlerType.OnHomePage,
       request: {
         jsonrpc: '2.0',
@@ -3686,7 +3687,7 @@ describe('SnapController', () => {
     await expect(
       snapController.handleRequest({
         snapId: MOCK_SNAP_ID,
-        origin: MOCK_ORIGIN,
+        origin: METAMASK_ORIGIN,
         handler: HandlerType.OnSettingsPage,
         request: {
           jsonrpc: '2.0',
@@ -3740,7 +3741,7 @@ describe('SnapController', () => {
     await expect(
       snapController.handleRequest({
         snapId: MOCK_SNAP_ID,
-        origin: MOCK_ORIGIN,
+        origin: METAMASK_ORIGIN,
         handler: HandlerType.OnSettingsPage,
         request: {
           jsonrpc: '2.0',
@@ -3793,7 +3794,7 @@ describe('SnapController', () => {
 
     const result = await snapController.handleRequest({
       snapId: MOCK_SNAP_ID,
-      origin: MOCK_ORIGIN,
+      origin: METAMASK_ORIGIN,
       handler: HandlerType.OnSettingsPage,
       request: {
         jsonrpc: '2.0',
@@ -3849,7 +3850,7 @@ describe('SnapController', () => {
     await expect(
       snapController.handleRequest({
         snapId: MOCK_SNAP_ID,
-        origin: 'metamask',
+        origin: METAMASK_ORIGIN,
         handler: HandlerType.OnNameLookup,
         request: {
           jsonrpc: '2.0',
@@ -3912,7 +3913,7 @@ describe('SnapController', () => {
 
     const result = await snapController.handleRequest({
       snapId: MOCK_SNAP_ID,
-      origin: MOCK_ORIGIN,
+      origin: METAMASK_ORIGIN,
       handler: HandlerType.OnNameLookup,
       request: {
         jsonrpc: '2.0',
@@ -3965,7 +3966,7 @@ describe('SnapController', () => {
     expect(
       await snapController.handleRequest({
         snapId: MOCK_SNAP_ID,
-        origin: MOCK_ORIGIN,
+        origin: METAMASK_ORIGIN,
         handler: HandlerType.OnNameLookup,
         request: {
           jsonrpc: '2.0',
@@ -4026,7 +4027,7 @@ describe('SnapController', () => {
       await expect(
         snapController.handleRequest({
           snapId: MOCK_SNAP_ID,
-          origin: MOCK_ORIGIN,
+          origin: METAMASK_ORIGIN,
           handler: HandlerType.OnAssetsLookup,
           request: {
             jsonrpc: '2.0',
@@ -4102,7 +4103,7 @@ describe('SnapController', () => {
       expect(
         await snapController.handleRequest({
           snapId: MOCK_SNAP_ID,
-          origin: MOCK_ORIGIN,
+          origin: METAMASK_ORIGIN,
           handler: HandlerType.OnAssetsLookup,
           request: {
             jsonrpc: '2.0',
@@ -4178,7 +4179,7 @@ describe('SnapController', () => {
       expect(
         await snapController.handleRequest({
           snapId: MOCK_SNAP_ID,
-          origin: MOCK_ORIGIN,
+          origin: METAMASK_ORIGIN,
           handler: HandlerType.OnAssetsLookup,
           request: {
             jsonrpc: '2.0',
@@ -4258,7 +4259,7 @@ describe('SnapController', () => {
       await expect(
         snapController.handleRequest({
           snapId: MOCK_SNAP_ID,
-          origin: MOCK_ORIGIN,
+          origin: METAMASK_ORIGIN,
           handler: HandlerType.OnAssetsConversion,
           request: {
             jsonrpc: '2.0',
@@ -4327,7 +4328,7 @@ describe('SnapController', () => {
       expect(
         await snapController.handleRequest({
           snapId: MOCK_SNAP_ID,
-          origin: MOCK_ORIGIN,
+          origin: METAMASK_ORIGIN,
           handler: HandlerType.OnAssetsConversion,
           request: {
             jsonrpc: '2.0',
@@ -4401,7 +4402,7 @@ describe('SnapController', () => {
       expect(
         await snapController.handleRequest({
           snapId: MOCK_SNAP_ID,
-          origin: MOCK_ORIGIN,
+          origin: METAMASK_ORIGIN,
           handler: HandlerType.OnAssetsConversion,
           request: {
             jsonrpc: '2.0',
@@ -4492,7 +4493,7 @@ describe('SnapController', () => {
       expect(
         await snapController.handleRequest({
           snapId: MOCK_SNAP_ID,
-          origin: MOCK_ORIGIN,
+          origin: METAMASK_ORIGIN,
           handler: HandlerType.OnAssetsConversion,
           request: {
             jsonrpc: '2.0',
@@ -4579,7 +4580,7 @@ describe('SnapController', () => {
       await expect(
         snapController.handleRequest({
           snapId: MOCK_SNAP_ID,
-          origin: MOCK_ORIGIN,
+          origin: METAMASK_ORIGIN,
           handler: HandlerType.OnAssetHistoricalPrice,
           request: {
             jsonrpc: '2.0',
@@ -4646,7 +4647,7 @@ describe('SnapController', () => {
       expect(
         await snapController.handleRequest({
           snapId: MOCK_SNAP_ID,
-          origin: MOCK_ORIGIN,
+          origin: METAMASK_ORIGIN,
           handler: HandlerType.OnAssetHistoricalPrice,
           request: {
             jsonrpc: '2.0',
@@ -4671,6 +4672,93 @@ describe('SnapController', () => {
     });
   });
 
+  describe('onClientRequest', () => {
+    it('returns the value when `onClientRequest` returns a valid response', async () => {
+      const rootMessenger = getControllerMessenger();
+      const messenger = getSnapControllerMessenger(rootMessenger);
+      const snapController = getSnapController(
+        getSnapControllerOptions({
+          messenger,
+          state: {
+            snaps: getPersistedSnapsState(),
+          },
+        }),
+      );
+
+      rootMessenger.registerActionHandler(
+        'SubjectMetadataController:getSubjectMetadata',
+        () => MOCK_SNAP_SUBJECT_METADATA,
+      );
+
+      rootMessenger.registerActionHandler(
+        'ExecutionService:handleRpcRequest',
+        async () => ({
+          foo: 'bar',
+        }),
+      );
+
+      expect(
+        await snapController.handleRequest({
+          snapId: MOCK_SNAP_ID,
+          origin: METAMASK_ORIGIN,
+          handler: HandlerType.OnClientRequest,
+          request: {
+            jsonrpc: '2.0',
+            method: 'foo',
+            params: {},
+            id: 1,
+          },
+        }),
+      ).toStrictEqual({
+        foo: 'bar',
+      });
+
+      snapController.destroy();
+    });
+
+    it('throws if the origin is not "metamask"', async () => {
+      const rootMessenger = getControllerMessenger();
+      const messenger = getSnapControllerMessenger(rootMessenger);
+      const snapController = getSnapController(
+        getSnapControllerOptions({
+          messenger,
+          state: {
+            snaps: getPersistedSnapsState(),
+          },
+        }),
+      );
+
+      rootMessenger.registerActionHandler(
+        'SubjectMetadataController:getSubjectMetadata',
+        () => MOCK_SNAP_SUBJECT_METADATA,
+      );
+
+      rootMessenger.registerActionHandler(
+        'ExecutionService:handleRpcRequest',
+        async () =>
+          Promise.resolve({
+            foo: 'bar',
+          }),
+      );
+
+      await expect(
+        snapController.handleRequest({
+          snapId: MOCK_SNAP_ID,
+          origin: MOCK_ORIGIN,
+          handler: HandlerType.OnClientRequest,
+          request: {
+            jsonrpc: '2.0',
+            method: 'foo',
+            params: {},
+            id: 1,
+          },
+        }),
+      ).rejects.toThrow('"onClientRequest" can only be invoked by MetaMask.');
+
+      snapController.destroy();
+    });
+  });
+
   describe('getRpcRequestHandler', () => {
     it('handlers populate the "jsonrpc" property if missing', async () => {
       const rootMessenger = getControllerMessenger();
@@ -5661,7 +5749,7 @@ describe('SnapController', () => {
       expect(rootMessenger.publish).toHaveBeenCalledWith(
         'SnapController:snapInstalled',
         getTruncatedSnap(),
-        'metamask',
+        METAMASK_ORIGIN,
         true,
       );
 
@@ -5900,7 +5988,7 @@ describe('SnapController', () => {
           },
         }),
         '1.0.0',
-        'metamask',
+        METAMASK_ORIGIN,
         true,
       );
 
@@ -9478,7 +9566,7 @@ describe('SnapController', () => {
 
         await snapController.handleRequest({
           snapId: snap.id,
-          origin: MOCK_ORIGIN,
+          origin: METAMASK_ORIGIN,
           handler: HandlerType.OnCronjob,
           request: {
             jsonrpc: '2.0',
@@ -9656,7 +9744,7 @@ describe('SnapController', () => {
         await messenger.call('SnapController:handleRequest', {
           snapId: MOCK_SNAP_ID,
           handler: HandlerType.OnNameLookup,
-          origin: 'metamask',
+          origin: METAMASK_ORIGIN,
           request: {},
         }),
       ).toBe(true);
@@ -10923,7 +11011,7 @@ describe('SnapController', () => {
         MOCK_SNAP_ID,
         {
           handler: HandlerType.OnInstall,
-          origin: 'metamask',
+          origin: METAMASK_ORIGIN,
           request: {
             jsonrpc: '2.0',
             id: expect.any(String),
@@ -11066,7 +11154,7 @@ describe('SnapController', () => {
         MOCK_SNAP_ID,
         {
           handler: HandlerType.OnUpdate,
-          origin: 'metamask',
+          origin: METAMASK_ORIGIN,
           request: {
             jsonrpc: '2.0',
             id: expect.any(String),
diff --git a/packages/snaps-controllers/src/snaps/SnapController.ts b/packages/snaps-controllers/src/snaps/SnapController.ts
index 805a6fd827..c7739fba54 100644
--- a/packages/snaps-controllers/src/snaps/SnapController.ts
+++ b/packages/snaps-controllers/src/snaps/SnapController.ts
@@ -136,7 +136,9 @@ import { gt } from 'semver';
 
 import {
   ALLOWED_PERMISSIONS,
+  CLIENT_ONLY_HANDLERS,
   LEGACY_ENCRYPTION_KEY_DERIVATION_OPTIONS,
+  METAMASK_ORIGIN,
   STATE_DEBOUNCE_TIMEOUT,
 } from './constants';
 import type { SnapLocation } from './location';
@@ -1311,7 +1313,7 @@ export class SnapController extends BaseController<
       // Add snap to the SnapController state
       this.#set({
         id: snapId,
-        origin: 'metamask',
+        origin: METAMASK_ORIGIN,
         files: filesObject,
         removable,
         hidden,
@@ -1350,14 +1352,14 @@ export class SnapController extends BaseController<
           'SnapController:snapUpdated',
           this.getTruncatedExpect(snapId),
           existingSnap.version,
-          'metamask',
+          METAMASK_ORIGIN,
           true,
         );
       } else {
         this.messagingSystem.publish(
           'SnapController:snapInstalled',
           this.getTruncatedExpect(snapId),
-          'metamask',
+          METAMASK_ORIGIN,
           true,
         );
       }
@@ -3415,7 +3417,7 @@ export class SnapController extends BaseController<
     this.#assertCanUsePlatform();
 
     assert(
-      origin === 'metamask' || isValidUrl(origin),
+      origin === METAMASK_ORIGIN || isValidUrl(origin),
       "'origin' must be a valid URL or 'metamask'.",
     );
 
@@ -3485,6 +3487,13 @@ export class SnapController extends BaseController<
       }
     }
 
+    if (
+      origin !== METAMASK_ORIGIN &&
+      CLIENT_ONLY_HANDLERS.includes(handlerType)
+    ) {
+      throw new Error(`"${handlerType}" can only be invoked by MetaMask.`);
+    }
+
     const handler = this.#getRpcRequestHandler(snapId);
     if (!handler) {
       throw new Error(
diff --git a/packages/snaps-controllers/src/snaps/constants.ts b/packages/snaps-controllers/src/snaps/constants.ts
index dfaaa88ad3..0d380ad015 100644
--- a/packages/snaps-controllers/src/snaps/constants.ts
+++ b/packages/snaps-controllers/src/snaps/constants.ts
@@ -1,4 +1,5 @@
 import { SnapEndowments } from '@metamask/snaps-rpc-methods';
+import { HandlerType } from '@metamask/snaps-utils';
 
 // These permissions are allowed without being on the allowlist.
 export const ALLOWED_PERMISSIONS = Object.freeze([
@@ -25,3 +26,21 @@ export const LEGACY_ENCRYPTION_KEY_DERIVATION_OPTIONS = {
  * The timeout for debouncing state updates.
  */
 export const STATE_DEBOUNCE_TIMEOUT = 500;
+
+// The origin used to indicate requests coming from the client.
+export const METAMASK_ORIGIN = 'metamask';
+
+// These handlers are only allowed to be invoked by the client.
+export const CLIENT_ONLY_HANDLERS = Object.freeze([
+  HandlerType.OnClientRequest,
+  HandlerType.OnSignature,
+  HandlerType.OnTransaction,
+  HandlerType.OnCronjob,
+  HandlerType.OnNameLookup,
+  HandlerType.OnHomePage,
+  HandlerType.OnSettingsPage,
+  HandlerType.OnUserInput,
+  HandlerType.OnAssetsLookup,
+  HandlerType.OnAssetsConversion,
+  HandlerType.OnAssetHistoricalPrice,
+]);
diff --git a/packages/snaps-execution-environments/coverage.json b/packages/snaps-execution-environments/coverage.json
index a805965c70..47984c18cf 100644
--- a/packages/snaps-execution-environments/coverage.json
+++ b/packages/snaps-execution-environments/coverage.json
@@ -1,6 +1,6 @@
 {
-  "branches": 90,
+  "branches": 90.04,
   "functions": 94.57,
-  "lines": 90.15,
-  "statements": 89.52
+  "lines": 90.16,
+  "statements": 89.53
 }
diff --git a/packages/snaps-execution-environments/src/common/BaseSnapExecutor.test.browser.ts b/packages/snaps-execution-environments/src/common/BaseSnapExecutor.test.browser.ts
index a1f673c48e..c39bcfed8a 100644
--- a/packages/snaps-execution-environments/src/common/BaseSnapExecutor.test.browser.ts
+++ b/packages/snaps-execution-environments/src/common/BaseSnapExecutor.test.browser.ts
@@ -1821,6 +1821,39 @@ describe('BaseSnapExecutor', () => {
     });
   });
 
+  it('supports onClientRequest export', async () => {
+    const CODE = `
+      module.exports.onClientRequest = ({ request }) => ({ request });
+    `;
+
+    const executor = new TestSnapExecutor();
+    await executor.executeSnap(1, MOCK_SNAP_ID, CODE, []);
+
+    expect(await executor.readCommand()).toStrictEqual({
+      jsonrpc: '2.0',
+      id: 1,
+      result: 'OK',
+    });
+
+    await executor.writeCommand({
+      jsonrpc: '2.0',
+      id: 2,
+      method: 'snapRpc',
+      params: [
+        MOCK_SNAP_ID,
+        HandlerType.OnClientRequest,
+        MOCK_ORIGIN,
+        { jsonrpc: '2.0', method: 'foo', params: [] },
+      ],
+    });
+
+    expect(await executor.readCommand()).toStrictEqual({
+      id: 2,
+      jsonrpc: '2.0',
+      result: { request: { jsonrpc: '2.0', method: 'foo', params: [] } },
+    });
+  });
+
   describe('lifecycle hooks', () => {
     const LIFECYCLE_HOOKS = [HandlerType.OnInstall, HandlerType.OnUpdate];
 
diff --git a/packages/snaps-execution-environments/src/common/commands.ts b/packages/snaps-execution-environments/src/common/commands.ts
index 333ab29897..6d42a8cb9c 100644
--- a/packages/snaps-execution-environments/src/common/commands.ts
+++ b/packages/snaps-execution-environments/src/common/commands.ts
@@ -107,6 +107,7 @@ export function getHandlerArguments(
     case HandlerType.OnKeyringRequest:
       return { origin, request };
 
+    case HandlerType.OnClientRequest:
     case HandlerType.OnCronjob:
       return { request };
 
diff --git a/packages/snaps-rpc-methods/src/endowments/index.ts b/packages/snaps-rpc-methods/src/endowments/index.ts
index 60c68b1c01..7e460241fd 100644
--- a/packages/snaps-rpc-methods/src/endowments/index.ts
+++ b/packages/snaps-rpc-methods/src/endowments/index.ts
@@ -130,6 +130,7 @@ export const handlerEndowments: Record<HandlerType, string | null> = {
   [HandlerType.OnAssetsLookup]: assetsEndowmentBuilder.targetName,
   [HandlerType.OnAssetsConversion]: assetsEndowmentBuilder.targetName,
   [HandlerType.OnProtocolRequest]: protocolEndowmentBuilder.targetName,
+  [HandlerType.OnClientRequest]: null,
 };
 
 export * from './enum';
diff --git a/packages/snaps-sdk/src/types/handlers/client-request.ts b/packages/snaps-sdk/src/types/handlers/client-request.ts
new file mode 100644
index 0000000000..50e216aa28
--- /dev/null
+++ b/packages/snaps-sdk/src/types/handlers/client-request.ts
@@ -0,0 +1,16 @@
+import type { Json, JsonRpcParams, JsonRpcRequest } from '@metamask/utils';
+
+/**
+ * The `onClientRequest` handler, which is called when a Snap receives a JSON-RPC
+ * request from the client exclusively.
+ *
+ * @param args - The request arguments.
+ * @param args.request - The JSON-RPC request sent to the snap. This includes
+ * the method name and parameters.
+ * @returns The response to the JSON-RPC request. This must be a
+ * JSON-serializable value. In order to return an error, throw a `SnapError`
+ * instead.
+ */
+export type OnClientRequestHandler<
+  Params extends JsonRpcParams = JsonRpcParams,
+> = (args: { request: JsonRpcRequest<Params> }) => Promise<Json>;
diff --git a/packages/snaps-sdk/src/types/handlers/index.ts b/packages/snaps-sdk/src/types/handlers/index.ts
index 470fa182e2..d8049efac4 100644
--- a/packages/snaps-sdk/src/types/handlers/index.ts
+++ b/packages/snaps-sdk/src/types/handlers/index.ts
@@ -1,6 +1,7 @@
 export type * from './asset-historical-price';
 export type * from './assets-conversion';
 export * from './assets-lookup';
+export type * from './client-request';
 export type * from './cronjob';
 export type * from './home-page';
 export type * from './keyring';
diff --git a/packages/snaps-utils/coverage.json b/packages/snaps-utils/coverage.json
index 3a08980160..0141f93a65 100644
--- a/packages/snaps-utils/coverage.json
+++ b/packages/snaps-utils/coverage.json
@@ -2,5 +2,5 @@
   "branches": 99.75,
   "functions": 98.95,
   "lines": 98.57,
-  "statements": 97.07
+  "statements": 97.08
 }
diff --git a/packages/snaps-utils/src/handlers/exports.test.ts b/packages/snaps-utils/src/handlers/exports.test.ts
index 3f1d445147..ad927a2198 100644
--- a/packages/snaps-utils/src/handlers/exports.test.ts
+++ b/packages/snaps-utils/src/handlers/exports.test.ts
@@ -30,6 +30,7 @@ describe('SNAP_EXPORT_NAMES', () => {
       'onAssetsConversion',
       'onAssetHistoricalPrice',
       'onProtocolRequest',
+      'onClientRequest',
     ]);
   });
 });
diff --git a/packages/snaps-utils/src/handlers/exports.ts b/packages/snaps-utils/src/handlers/exports.ts
index e9e491b68d..6e47244992 100644
--- a/packages/snaps-utils/src/handlers/exports.ts
+++ b/packages/snaps-utils/src/handlers/exports.ts
@@ -2,6 +2,7 @@ import type {
   OnAssetHistoricalPriceHandler,
   OnAssetsConversionHandler,
   OnAssetsLookupHandler,
+  OnClientRequestHandler,
   OnCronjobHandler,
   OnHomePageHandler,
   OnInstallHandler,
@@ -130,6 +131,13 @@ export const SNAP_EXPORTS = {
       return typeof snapExport === 'function';
     },
   },
+  [HandlerType.OnClientRequest]: {
+    type: HandlerType.OnClientRequest,
+    required: true,
+    validator: (snapExport: unknown): snapExport is OnClientRequestHandler => {
+      return typeof snapExport === 'function';
+    },
+  },
 } as const;
 
 export const SNAP_EXPORT_NAMES = Object.values(HandlerType);
diff --git a/packages/snaps-utils/src/handlers/types.ts b/packages/snaps-utils/src/handlers/types.ts
index 882893e303..d6ddb7fd57 100644
--- a/packages/snaps-utils/src/handlers/types.ts
+++ b/packages/snaps-utils/src/handlers/types.ts
@@ -44,6 +44,7 @@ export enum HandlerType {
   OnAssetsConversion = 'onAssetsConversion',
   OnAssetHistoricalPrice = 'onAssetHistoricalPrice',
   OnProtocolRequest = 'onProtocolRequest',
+  OnClientRequest = 'onClientRequest',
 }
 
 export type SnapHandler = {