diff --git a/packages/snaps-jest/src/internals/request.test.tsx b/packages/snaps-jest/src/internals/request.test.tsx
index 49abb716ed..a9c5883073 100644
--- a/packages/snaps-jest/src/internals/request.test.tsx
+++ b/packages/snaps-jest/src/internals/request.test.tsx
@@ -10,6 +10,7 @@ import {
   getRestrictedSnapInterfaceControllerMessenger,
   getRootControllerMessenger,
 } from '../test-utils';
+import type { SnapResponseWithInterface } from '../types';
 import {
   getInterfaceApi,
   getInterfaceFromResult,
@@ -97,6 +98,80 @@ describe('handleRequest', () => {
     await snap.executionService.terminateAllSnaps();
   });
 
+  it('gracefully handles returned invalid UI', async () => {
+    const controllerMessenger = getRootControllerMessenger();
+
+    const { snapId, close: closeServer } = await getMockServer({
+      sourceCode: `
+        module.exports.onHomePage = async (request) => {
+          return ({ content: 'foo' });
+        };
+      `,
+      port: 4242,
+    });
+
+    const snap = await handleInstallSnap(snapId);
+    const response = await handleRequest({
+      ...snap,
+      controllerMessenger,
+      handler: HandlerType.OnHomePage,
+      request: {
+        method: '',
+      },
+    });
+
+    expect(response).toStrictEqual({
+      id: expect.any(String),
+      response: {
+        error: expect.objectContaining({
+          code: -32603,
+          message: 'The Snap returned an invalid interface.',
+        }),
+      },
+      notifications: [],
+      getInterface: expect.any(Function),
+    });
+
+    expect(() =>
+      (response as SnapResponseWithInterface).getInterface(),
+    ).toThrow(
+      'Unable to get the interface from the Snap: The request to the Snap failed.',
+    );
+
+    await closeServer();
+    await snap.executionService.terminateAllSnaps();
+  });
+
+  it('gracefully handles returned invalid UI when not awaiting the request', async () => {
+    const controllerMessenger = getRootControllerMessenger();
+
+    const { snapId, close: closeServer } = await getMockServer({
+      sourceCode: `
+        module.exports.onHomePage = async (request) => {
+          return ({ content: 'foo' });
+        };
+      `,
+      port: 4242,
+    });
+
+    const snap = await handleInstallSnap(snapId);
+    const promise = handleRequest({
+      ...snap,
+      controllerMessenger,
+      handler: HandlerType.OnHomePage,
+      request: {
+        method: '',
+      },
+    });
+
+    await expect(promise.getInterface()).rejects.toThrow(
+      'Unable to get the interface from the Snap: The returned interface may be invalid. The error message received was: The Snap returned an invalid interface.',
+    );
+
+    await closeServer();
+    await snap.executionService.terminateAllSnaps();
+  });
+
   it('returns an error response', async () => {
     const { snapId, close: closeServer } = await getMockServer({
       sourceCode: `
@@ -125,6 +200,7 @@ describe('handleRequest', () => {
         }),
       },
       notifications: [],
+      getInterface: expect.any(Function),
     });
 
     await closeServer();
diff --git a/packages/snaps-jest/src/internals/request.ts b/packages/snaps-jest/src/internals/request.ts
index ee52b932e2..dae5083066 100644
--- a/packages/snaps-jest/src/internals/request.ts
+++ b/packages/snaps-jest/src/internals/request.ts
@@ -1,9 +1,20 @@
 import type { AbstractExecutionService } from '@metamask/snaps-controllers';
-import type { SnapId, Component } from '@metamask/snaps-sdk';
+import {
+  type SnapId,
+  type JsonRpcError,
+  type ComponentOrElement,
+  ComponentOrElementStruct,
+} from '@metamask/snaps-sdk';
 import type { HandlerType } from '@metamask/snaps-utils';
 import { unwrapError } from '@metamask/snaps-utils';
-import { getSafeJson, hasProperty, isPlainObject } from '@metamask/utils';
+import {
+  assert,
+  getSafeJson,
+  hasProperty,
+  isPlainObject,
+} from '@metamask/utils';
 import { nanoid } from '@reduxjs/toolkit';
+import { is } from 'superstruct';
 
 import type {
   RequestOptions,
@@ -20,6 +31,7 @@ import {
 } from './simulation';
 import type { RunSagaFunction, Store } from './simulation';
 import type { RootControllerMessenger } from './simulation/controllers';
+import { SnapResponseStruct } from './structs';
 
 export type HandleRequestOptions = {
   snapId: SnapId;
@@ -60,6 +72,12 @@ export function handleRequest({
   runSaga,
   request: { id = nanoid(), origin = 'https://metamask.io', ...options },
 }: HandleRequestOptions): SnapRequest {
+  const getInterfaceError = () => {
+    throw new Error(
+      'Unable to get the interface from the Snap: The request to the Snap failed.',
+    );
+  };
+
   const promise = executionService
     .handleRpcRequest(snapId, {
       origin,
@@ -74,20 +92,32 @@ export function handleRequest({
       const notifications = getNotifications(store.getState());
       store.dispatch(clearNotifications());
 
-      const getInterfaceFn = await getInterfaceApi(
-        result,
-        snapId,
-        controllerMessenger,
-      );
+      try {
+        const getInterfaceFn = await getInterfaceApi(
+          result,
+          snapId,
+          controllerMessenger,
+        );
 
-      return {
-        id: String(id),
-        response: {
-          result: getSafeJson(result),
-        },
-        notifications,
-        ...(getInterfaceFn ? { getInterface: getInterfaceFn } : {}),
-      };
+        return {
+          id: String(id),
+          response: {
+            result: getSafeJson(result),
+          },
+          notifications,
+          ...(getInterfaceFn ? { getInterface: getInterfaceFn } : {}),
+        };
+      } catch (error) {
+        const [unwrappedError] = unwrapError(error);
+        return {
+          id: String(id),
+          response: {
+            error: unwrappedError.serialize(),
+          },
+          notifications: [],
+          getInterface: getInterfaceError,
+        };
+      }
     })
     .catch((error) => {
       const [unwrappedError] = unwrapError(error);
@@ -98,16 +128,33 @@ export function handleRequest({
           error: unwrappedError.serialize(),
         },
         notifications: [],
+        getInterface: getInterfaceError,
       };
     }) as unknown as SnapRequest;
 
   promise.getInterface = async () => {
-    return await runSaga(
+    const sagaPromise = runSaga(
       getInterface,
       runSaga,
       snapId,
       controllerMessenger,
     ).toPromise();
+    const result = await Promise.race([promise, sagaPromise]);
+
+    // If the request promise has resolved to an error, we should throw
+    // instead of waiting for an interface that likely will never be displayed
+    if (
+      is(result, SnapResponseStruct) &&
+      hasProperty(result.response, 'error')
+    ) {
+      throw new Error(
+        `Unable to get the interface from the Snap: The returned interface may be invalid. The error message received was: ${
+          (result.response.error as JsonRpcError).message
+        }`,
+      );
+    }
+
+    return await sagaPromise;
   };
 
   return promise;
@@ -131,10 +178,14 @@ export async function getInterfaceFromResult(
   }
 
   if (isPlainObject(result) && hasProperty(result, 'content')) {
+    assert(
+      is(result.content, ComponentOrElementStruct),
+      'The Snap returned an invalid interface.',
+    );
     const id = await controllerMessenger.call(
       'SnapInterfaceController:createInterface',
       snapId,
-      result.content as Component,
+      result.content as ComponentOrElement,
     );
 
     return id;