diff --git a/.changeset/lemon-tigers-promise.md b/.changeset/lemon-tigers-promise.md
new file mode 100644
index 00000000000..7c397bae3ad
--- /dev/null
+++ b/.changeset/lemon-tigers-promise.md
@@ -0,0 +1,5 @@
+---
+"@apollo/client": patch
+---
+
+Start the query ref auto dispose timeout after the initial promise has settled. This prevents requests that run longer than the timeout duration from keeping the component suspended indefinitely.
diff --git a/.size-limit.cjs b/.size-limit.cjs
index d8da5ff2578..223a3dce7ae 100644
--- a/.size-limit.cjs
+++ b/.size-limit.cjs
@@ -1,7 +1,7 @@
 const checks = [
   {
     path: "dist/apollo-client.min.cjs",
-    limit: "37940",
+    limit: "37960",
   },
   {
     path: "dist/main.cjs",
diff --git a/src/react/cache/QueryReference.ts b/src/react/cache/QueryReference.ts
index 7a03ea10d37..f1ad5732bac 100644
--- a/src/react/cache/QueryReference.ts
+++ b/src/react/cache/QueryReference.ts
@@ -123,10 +123,19 @@ export class InternalQueryReference<TData = unknown> {
     // suspended resource does not use this queryRef in the given time. This
     // helps prevent memory leaks when a component has unmounted before the
     // query has finished loading.
-    this.autoDisposeTimeoutId = setTimeout(
-      this.dispose,
-      options.autoDisposeTimeoutMs ?? 30_000
-    );
+    const startDisposeTimer = () => {
+      if (!this.references) {
+        this.autoDisposeTimeoutId = setTimeout(
+          this.dispose,
+          options.autoDisposeTimeoutMs ?? 30_000
+        );
+      }
+    };
+
+    // We wait until the request has settled to ensure we don't dispose of the
+    // query ref before the request finishes, otherwise we would leave the
+    // promise in a pending state rendering the suspense boundary indefinitely.
+    this.promise.then(startDisposeTimer, startDisposeTimer);
   }
 
   get watchQueryOptions() {
diff --git a/src/react/hooks/__tests__/useSuspenseQuery.test.tsx b/src/react/hooks/__tests__/useSuspenseQuery.test.tsx
index 08b4abb3f64..468fe8f4fc5 100644
--- a/src/react/hooks/__tests__/useSuspenseQuery.test.tsx
+++ b/src/react/hooks/__tests__/useSuspenseQuery.test.tsx
@@ -805,8 +805,12 @@ describe("useSuspenseQuery", () => {
 
     expect(screen.queryByText("Loading greeting...")).not.toBeInTheDocument();
 
-    link.simulateResult({ result: { data: { greeting: "Hello" } } });
-    link.simulateComplete();
+    await act(() => {
+      link.simulateResult({ result: { data: { greeting: "Hello" } } }, true);
+      // Ensure simulateResult will deliver the result since its wrapped with
+      // setTimeout
+      jest.advanceTimersByTime(10);
+    });
 
     expect(client.getObservableQueries().size).toBe(1);
     expect(client).toHaveSuspenseCacheEntryUsing(query);
@@ -817,10 +821,6 @@ describe("useSuspenseQuery", () => {
     expect(client).not.toHaveSuspenseCacheEntryUsing(query);
 
     jest.useRealTimers();
-
-    // Avoid act warnings for a suspended resource
-    // eslint-disable-next-line testing-library/no-unnecessary-act
-    await act(() => wait(0));
   });
 
   it("has configurable auto dispose timer if the component never renders again after suspending", async () => {
@@ -871,8 +871,12 @@ describe("useSuspenseQuery", () => {
 
     expect(screen.queryByText("Loading greeting...")).not.toBeInTheDocument();
 
-    link.simulateResult({ result: { data: { greeting: "Hello" } } });
-    link.simulateComplete();
+    await act(() => {
+      link.simulateResult({ result: { data: { greeting: "Hello" } } }, true);
+      // Ensure simulateResult will deliver the result since its wrapped with
+      // setTimeout
+      jest.advanceTimersByTime(10);
+    });
 
     expect(client.getObservableQueries().size).toBe(1);
     expect(client).toHaveSuspenseCacheEntryUsing(query);
@@ -883,10 +887,6 @@ describe("useSuspenseQuery", () => {
     expect(client).not.toHaveSuspenseCacheEntryUsing(query);
 
     jest.useRealTimers();
-
-    // Avoid act warnings for a suspended resource
-    // eslint-disable-next-line testing-library/no-unnecessary-act
-    await act(() => wait(0));
   });
 
   it("cancels auto dispose if the component renders before timer finishes", async () => {
@@ -940,6 +940,57 @@ describe("useSuspenseQuery", () => {
     jest.useRealTimers();
   });
 
+  // https://github.com/apollographql/apollo-client/issues/11270
+  it("does not leave component suspended if query completes if request takes longer than auto dispose timeout", async () => {
+    jest.useFakeTimers();
+    const { query } = useSimpleQueryCase();
+    const link = new MockSubscriptionLink();
+    const client = new ApolloClient({
+      link,
+      cache: new InMemoryCache(),
+      defaultOptions: {
+        react: {
+          suspense: {
+            autoDisposeTimeoutMs: 10,
+          },
+        },
+      },
+    });
+
+    function App() {
+      return (
+        <ApolloProvider client={client}>
+          <Suspense fallback="Loading greeting...">
+            <Greeting />
+          </Suspense>
+        </ApolloProvider>
+      );
+    }
+
+    function Greeting() {
+      const { data } = useSuspenseQuery(query);
+
+      return <span>{data.greeting}</span>;
+    }
+
+    render(<App />);
+
+    // Ensure <Greeting /> suspends immediately
+    expect(screen.getByText("Loading greeting...")).toBeInTheDocument();
+
+    jest.advanceTimersByTime(20);
+
+    link.simulateResult({ result: { data: { greeting: "Hello" } } }, true);
+
+    await waitFor(() => {
+      expect(screen.queryByText("Loading greeting...")).not.toBeInTheDocument();
+    });
+
+    expect(screen.getByText("Hello")).toBeInTheDocument();
+
+    jest.useRealTimers();
+  });
+
   it("allows the client to be overridden", async () => {
     const { query } = useSimpleQueryCase();