diff --git a/packages/server-utils/test/integrations/express-error-handler.test.ts b/packages/server-utils/test/integrations/express-error-handler.test.ts
index e64a847d4867..67c4d7c8e183 100644
--- a/packages/server-utils/test/integrations/express-error-handler.test.ts
+++ b/packages/server-utils/test/integrations/express-error-handler.test.ts
@@ -1,12 +1,28 @@
 import * as SentryCore from '@sentry/core';
 import { afterEach, beforeEach, describe, expect, it, type MockInstance, vi } from 'vitest';
+import { isExpressErrorHandled } from '../../src/integrations/express/error-handled';
+// oxlint-disable-next-line typescript/no-deprecated
+import { expressErrorHandler } from '../../src/integrations/express/error-handler';
 import { captureLayerError } from '../../src/integrations/express/instrumentation';
-import type { HandleChannelContext } from '../../src/integrations/express/types';
+import type { ExpressRequest, ExpressResponse, HandleChannelContext } from '../../src/integrations/express/types';
 
 function makeErrorData(error: unknown, span?: unknown): HandleChannelContext {
   return { error, _sentrySpan: span } as unknown as HandleChannelContext;
 }
 
+/** Express hands every layer `[req, res, next]`. Sentry reads the request from there and marks it as handled. */
+function makeLayerErrorData(error: unknown, request: ExpressRequest, span?: unknown): HandleChannelContext {
+  return { error, _sentrySpan: span, arguments: [request] } as unknown as HandleChannelContext;
+}
+
+function makeRequest(): ExpressRequest {
+  return {
+    method: 'GET',
+    originalUrl: '/users/42?include=profile',
+    headers: { host: 'api.example.com', 'user-agent': 'vitest' },
+  } as unknown as ExpressRequest;
+}
+
 describe('captureLayerError', () => {
   let captureExceptionSpy: MockInstance;
 
@@ -110,4 +126,158 @@ describe('captureLayerError', () => {
     expect(withActiveSpanSpy).not.toHaveBeenCalled();
     expect(captureExceptionSpy).toHaveBeenCalledTimes(1);
   });
+
+  describe('per-request dedup marker', () => {
+    it('captures once when the same error bubbles through several layers', () => {
+      const request = makeRequest();
+      const error = Object.assign(new Error('boom'), { statusCode: 500 });
+
+      captureLayerError(makeLayerErrorData(error, request), undefined);
+      captureLayerError(makeLayerErrorData(error, request), undefined);
+      captureLayerError(makeLayerErrorData(error, request), undefined);
+
+      expect(captureExceptionSpy).toHaveBeenCalledTimes(1);
+    });
+
+    it('marks the request when the error is skipped, so the deprecated middleware defers', () => {
+      const request = makeRequest();
+      const error = Object.assign(new Error('bad request'), { statusCode: 400 });
+
+      captureLayerError(makeLayerErrorData(error, request), undefined);
+
+      expect(captureExceptionSpy).not.toHaveBeenCalled();
+      expect(isExpressErrorHandled(request)).toBe(true);
+    });
+
+    it('marks the request when shouldHandleError is false', () => {
+      const request = makeRequest();
+      const error = Object.assign(new Error('boom'), { statusCode: 500 });
+
+      captureLayerError(makeLayerErrorData(error, request), false);
+
+      expect(captureExceptionSpy).not.toHaveBeenCalled();
+      expect(isExpressErrorHandled(request)).toBe(true);
+    });
+
+    it('leaves the request unmarked when there is no error', () => {
+      const request = makeRequest();
+
+      captureLayerError(makeLayerErrorData(undefined, request), undefined);
+
+      expect(isExpressErrorHandled(request)).toBe(false);
+    });
+
+    // No request means nothing to mark, so every layer captures again. Express always passes one, so this cannot happen in practice.
+    it('captures on every layer when Express passes no request', () => {
+      const error = Object.assign(new Error('boom'), { statusCode: 500 });
+
+      captureLayerError(makeErrorData(error), undefined);
+      captureLayerError(makeErrorData(error), undefined);
+
+      expect(captureExceptionSpy).toHaveBeenCalledTimes(2);
+    });
+
+    // TODO: Sentry marks the request, not the error, so only the first error per request is captured. Later errors on the same request are lost.
+    it.fails('captures a second, distinct error raised on the same request', () => {
+      const request = makeRequest();
+      const firstError = Object.assign(new Error('first failure'), { statusCode: 400 });
+      const secondError = Object.assign(new Error('second failure'), { statusCode: 500 });
+
+      captureLayerError(makeLayerErrorData(firstError, request), undefined);
+      captureLayerError(makeLayerErrorData(secondError, request), undefined);
+
+      expect(captureExceptionSpy).toHaveBeenCalledWith(secondError, {
+        mechanism: { type: 'auto.http.express', handled: false },
+      });
+    });
+  });
+});
+
+describe('expressErrorHandler', () => {
+  let captureExceptionSpy: MockInstance;
+
+  beforeEach(() => {
+    captureExceptionSpy = vi.spyOn(SentryCore, 'captureException').mockImplementation(() => 'event-id');
+  });
+
+  afterEach(() => {
+    vi.restoreAllMocks();
+  });
+
+  function makeResponse(): ExpressResponse & { sentry?: string } {
+    return { once: () => undefined, removeListener: () => undefined } as unknown as ExpressResponse & {
+      sentry?: string;
+    };
+  }
+
+  // A request whose error the integration already captured, before this middleware runs.
+  function makeHandledRequest(): ExpressRequest {
+    const request = makeRequest();
+    captureLayerError(makeLayerErrorData(new Error('captured by the integration'), request), undefined);
+    return request;
+  }
+
+  it('captures a 5xx error and exposes the event id on the response', () => {
+    const res = makeResponse();
+    const error = Object.assign(new Error('boom'), { statusCode: 500 });
+
+    expressErrorHandler()(error, makeRequest(), res, vi.fn());
+
+    expect(captureExceptionSpy).toHaveBeenCalledWith(error, {
+      mechanism: { type: 'auto.middleware.express', handled: false },
+    });
+    expect(res.sentry).toBe('event-id');
+  });
+
+  it('does not capture a 4xx error', () => {
+    const res = makeResponse();
+    const error = Object.assign(new Error('bad request'), { statusCode: 400 });
+
+    expressErrorHandler()(error, makeRequest(), res, vi.fn());
+
+    expect(captureExceptionSpy).not.toHaveBeenCalled();
+    expect(res.sentry).toBeUndefined();
+  });
+
+  it.each([
+    ['captured', 500],
+    ['skipped', 400],
+  ])('forwards the error to next when %s', (_case, statusCode) => {
+    const next = vi.fn();
+    const error = Object.assign(new Error('boom'), { statusCode });
+
+    expressErrorHandler()(error, makeRequest(), makeResponse(), next);
+
+    expect(next).toHaveBeenCalledExactlyOnceWith(error);
+  });
+
+  it('defers to the integration once the request is marked', () => {
+    const request = makeHandledRequest();
+    captureExceptionSpy.mockClear();
+    const error = Object.assign(new Error('boom'), { statusCode: 500 });
+
+    expressErrorHandler()(error, request, makeResponse(), vi.fn());
+
+    expect(captureExceptionSpy).not.toHaveBeenCalled();
+  });
+
+  it('forwards the error to next even when it defers', () => {
+    const next = vi.fn();
+    const error = Object.assign(new Error('boom'), { statusCode: 500 });
+
+    expressErrorHandler()(error, makeHandledRequest(), makeResponse(), next);
+
+    expect(next).toHaveBeenCalledExactlyOnceWith(error);
+  });
+
+  // TODO: `res.sentry` carries the captured event id, but only this middleware sets it.
+  //  Once the integration captures first, apps reading `res.sentry` get undefined instead of the id.
+  it.fails('exposes the event id on the response when the integration captured the error', () => {
+    const res = makeResponse();
+    const error = Object.assign(new Error('boom'), { statusCode: 500 });
+
+    expressErrorHandler()(error, makeHandledRequest(), res, vi.fn());
+
+    expect(res.sentry).toBe('event-id');
+  });
 });