diff --git a/packages/snaps-controllers/coverage.json b/packages/snaps-controllers/coverage.json
index f9a4bdc274..bf7d34a45b 100644
--- a/packages/snaps-controllers/coverage.json
+++ b/packages/snaps-controllers/coverage.json
@@ -1,5 +1,5 @@
 {
-  "branches": 93.44,
+  "branches": 93.48,
   "functions": 97.38,
   "lines": 98.34,
   "statements": 98.08
diff --git a/packages/snaps-controllers/src/snaps/SnapController.test.tsx b/packages/snaps-controllers/src/snaps/SnapController.test.tsx
index 6cf674e691..2812bd541a 100644
--- a/packages/snaps-controllers/src/snaps/SnapController.test.tsx
+++ b/packages/snaps-controllers/src/snaps/SnapController.test.tsx
@@ -19,8 +19,12 @@ import {
   SnapEndowments,
 } from '@metamask/snaps-rpc-methods';
 import type { SnapId } from '@metamask/snaps-sdk';
-import { AuxiliaryFileEncoding, text } from '@metamask/snaps-sdk';
-import { Text } from '@metamask/snaps-sdk/jsx';
+import {
+  AuxiliaryFileEncoding,
+  text,
+  UserInputEventType,
+} from '@metamask/snaps-sdk';
+import { Text, Box, Button } from '@metamask/snaps-sdk/jsx';
 import type { SnapPermissions, RpcOrigins } from '@metamask/snaps-utils';
 import {
   getPlatformVersion,
@@ -2242,7 +2246,11 @@ describe('SnapController', () => {
           snapId: snap.id,
           origin: MOCK_ORIGIN,
           handler: HandlerType.OnUserInput,
-          request: { jsonrpc: '2.0', method: 'test' },
+          request: {
+            jsonrpc: '2.0',
+            method: 'test',
+            params: { id: MOCK_INTERFACE_ID },
+          },
         }),
       ).toBeUndefined();
 
@@ -2770,6 +2778,77 @@ describe('SnapController', () => {
       snapController.destroy();
     });
 
+    it('injects context into onUserInput', async () => {
+      const rootMessenger = getControllerMessenger();
+      const messenger = getSnapControllerMessenger(rootMessenger);
+      const snapController = getSnapController(
+        getSnapControllerOptions({
+          messenger,
+          state: {
+            snaps: getPersistedSnapsState(),
+          },
+        }),
+      );
+
+      rootMessenger.registerActionHandler(
+        'SnapInterfaceController:getInterface',
+        () => ({
+          id: MOCK_INTERFACE_ID,
+          snapId: MOCK_SNAP_ID,
+          content: (
+            <Box>
+              <Button name="button">Click me</Button>
+            </Box>
+          ),
+          state: {},
+          context: { foo: 'bar' },
+          contentType: null,
+        }),
+      );
+
+      await snapController.handleRequest({
+        snapId: MOCK_SNAP_ID,
+        origin: MOCK_ORIGIN,
+        handler: HandlerType.OnUserInput,
+        request: {
+          jsonrpc: '2.0',
+          method: ' ',
+          params: {
+            id: MOCK_INTERFACE_ID,
+            event: {
+              type: UserInputEventType.ButtonClickEvent,
+              name: 'button',
+            },
+          },
+        },
+      });
+
+      expect(rootMessenger.call).toHaveBeenNthCalledWith(
+        4,
+        'ExecutionService:handleRpcRequest',
+        MOCK_SNAP_ID,
+        {
+          origin: MOCK_ORIGIN,
+          handler: HandlerType.OnUserInput,
+          request: {
+            id: expect.any(String),
+            method: ' ',
+            jsonrpc: '2.0',
+            params: {
+              id: MOCK_INTERFACE_ID,
+              event: {
+                type: UserInputEventType.ButtonClickEvent,
+                name: 'button',
+              },
+              context: { foo: 'bar' },
+            },
+          },
+        },
+      );
+
+      snapController.destroy();
+    });
+
     it('throws if onTransaction handler returns a phishing link', async () => {
       const rootMessenger = getControllerMessenger();
       const messenger = getSnapControllerMessenger(rootMessenger);
diff --git a/packages/snaps-controllers/src/snaps/SnapController.ts b/packages/snaps-controllers/src/snaps/SnapController.ts
index 49c7cdf5e1..c36bd8fb71 100644
--- a/packages/snaps-controllers/src/snaps/SnapController.ts
+++ b/packages/snaps-controllers/src/snaps/SnapController.ts
@@ -111,6 +111,7 @@ import type {
   NonEmptyArray,
   SemVerRange,
   CaipAssetType,
+  JsonRpcRequest,
 } from '@metamask/utils';
 import {
   assert,
@@ -213,7 +214,7 @@ export type PreinstalledSnap = {
 };
 
 type SnapRpcHandler = (
-  options: SnapRpcHookArgs & { timeout: number },
+  options: SnapRpcHookArgs & { timeout: number; request: JsonRpcRequest },
 ) => Promise<unknown>;
 
 /**
@@ -3513,7 +3514,7 @@ export class SnapController extends BaseController<
       handler: handlerType,
       request,
       timeout,
-    }: SnapRpcHookArgs & { timeout: number }) => {
+    }: SnapRpcHookArgs & { timeout: number; request: JsonRpcRequest }) => {
       if (!this.state.snaps[snapId].enabled) {
         throw new Error(`Snap "${snapId}" is disabled.`);
       }
@@ -3547,13 +3548,19 @@ export class SnapController extends BaseController<
         }
       }
 
+      const transformedRequest = this.#transformSnapRpcRequest(
+        snapId,
+        handlerType,
+        request,
+      );
+
       const timer = new Timer(timeout);
-      this.#recordSnapRpcRequestStart(snapId, request.id, timer);
+      this.#recordSnapRpcRequestStart(snapId, transformedRequest.id, timer);
 
       const handleRpcRequestPromise = this.messagingSystem.call(
         'ExecutionService:handleRpcRequest',
         snapId,
-        { origin, handler: handlerType, request },
+        { origin, handler: handlerType, request: transformedRequest },
       );
 
       // This will either get the result or reject due to the timeout.
@@ -3566,21 +3573,21 @@ export class SnapController extends BaseController<
           );
         }
 
-        await this.#assertSnapRpcRequestResult(snapId, handlerType, result);
+        await this.#assertSnapRpcResponse(snapId, handlerType, result);
 
-        const transformedResult = await this.#transformSnapRpcRequestResult(
+        const transformedResult = await this.#transformSnapRpcResponse(
           snapId,
           handlerType,
-          request,
+          transformedRequest,
           result,
         );
 
-        this.#recordSnapRpcRequestFinish(snapId, request.id);
+        this.#recordSnapRpcRequestFinish(snapId, transformedRequest.id);
 
         return transformedResult;
       } catch (error) {
         // We flag the RPC request as finished early since termination may affect pending requests
-        this.#recordSnapRpcRequestFinish(snapId, request.id);
+        this.#recordSnapRpcRequestFinish(snapId, transformedRequest.id);
         const [jsonRpcError, handled] = unwrapError(error);
 
         if (!handled) {
@@ -3629,15 +3636,15 @@ export class SnapController extends BaseController<
   }
 
   /**
-   * Transform a RPC request result if necessary.
+   * Transform a RPC response if necessary.
    *
    * @param snapId - The snap ID of the snap that produced the result.
    * @param handlerType - The handler type that produced the result.
    * @param request - The request that returned the result.
-   * @param result - The result.
+   * @param result - The response.
    * @returns The transformed result if applicable, otherwise the original result.
    */
-  async #transformSnapRpcRequestResult(
+  async #transformSnapRpcResponse(
     snapId: SnapId,
     handlerType: HandlerType,
     request: Record<string, unknown>,
@@ -3763,6 +3770,42 @@ export class SnapController extends BaseController<
     return { conversionRates: filteredConversionRates };
   }
 
+  /**
+   * Transforms a JSON-RPC request before sending it to the Snap, if required for a given handler.
+   *
+   * @param snapId - The Snap ID.
+   * @param handlerType - The handler being called.
+   * @param request - The JSON-RPC request.
+   * @returns The potentially transformed JSON-RPC request.
+   */
+  #transformSnapRpcRequest(
+    snapId: SnapId,
+    handlerType: HandlerType,
+    request: JsonRpcRequest,
+  ) {
+    switch (handlerType) {
+      // For onUserInput we inject context, so the client doesn't have to worry about keeping it in sync.
+      case HandlerType.OnUserInput: {
+        assert(request.params && hasProperty(request.params, 'id'));
+
+        const interfaceId = request.params.id as string;
+        const { context } = this.messagingSystem.call(
+          'SnapInterfaceController:getInterface',
+          snapId,
+          interfaceId,
+        );
+
+        return {
+          ...request,
+          params: { ...request.params, context },
+        };
+      }
+
+      default:
+        return request;
+    }
+  }
+
   /**
    * Assert that the returned result of a Snap RPC call is the expected shape.
    *
@@ -3770,7 +3813,7 @@ export class SnapController extends BaseController<
    * @param handlerType - The handler type of the RPC Request.
    * @param result - The result of the RPC request.
    */
-  async #assertSnapRpcRequestResult(
+  async #assertSnapRpcResponse(
     snapId: SnapId,
     handlerType: HandlerType,
     result: unknown,
diff --git a/packages/snaps-controllers/src/test-utils/controller.ts b/packages/snaps-controllers/src/test-utils/controller.ts
index f6c162cbb7..dfbfc27f2f 100644
--- a/packages/snaps-controllers/src/test-utils/controller.ts
+++ b/packages/snaps-controllers/src/test-utils/controller.ts
@@ -22,7 +22,8 @@ import {
   SnapEndowments,
   WALLET_SNAP_PERMISSION_KEY,
 } from '@metamask/snaps-rpc-methods';
-import type { SnapId, text } from '@metamask/snaps-sdk';
+import type { SnapId } from '@metamask/snaps-sdk';
+import { text } from '@metamask/snaps-sdk';
 import { SnapCaveatType } from '@metamask/snaps-utils';
 import {
   MockControllerMessenger,
@@ -440,7 +441,12 @@ export const getControllerMessenger = (registry = new MockSnapsRegistry()) => {
       if (id !== MOCK_INTERFACE_ID) {
         throw new Error(`Interface with id '${id}' not found.`);
       }
-      return { snapId, content: text('foo bar'), state: {} } as StoredInterface;
+      return {
+        snapId,
+        content: text('foo bar'),
+        state: {},
+        context: null,
+      } as StoredInterface;
     },
   );