diff --git a/packages/nextjs/src/config/templates/apiProxyLoaderTemplate.ts b/packages/nextjs/src/config/templates/apiProxyLoaderTemplate.ts
index 52bd696ece16..1cd7c40181eb 100644
--- a/packages/nextjs/src/config/templates/apiProxyLoaderTemplate.ts
+++ b/packages/nextjs/src/config/templates/apiProxyLoaderTemplate.ts
@@ -16,14 +16,29 @@ import type { PageConfig } from 'next';
 // multiple versions of next. See note in `wrappers/types` for more.
 import type { NextApiHandler } from '../wrappers';
 
-type NextApiModule = {
-  default: NextApiHandler;
-  config?: PageConfig;
-};
+type NextApiModule = (
+  | {
+      // ESM export
+      default?: NextApiHandler;
+    }
+  // CJS export
+  | NextApiHandler
+) & { config?: PageConfig };
 
 const userApiModule = origModule as NextApiModule;
 
-const maybeWrappedHandler = userApiModule.default;
+// Default to undefined. It's possible for Next.js users to not define any exports/handlers in an API route. If that is
+// the case Next.js wil crash during runtime but the Sentry SDK should definitely not crash so we need tohandle it.
+let userProvidedHandler = undefined;
+
+if ('default' in userApiModule && typeof userApiModule.default === 'function') {
+  // Handle when user defines via ESM export: `export default myFunction;`
+  userProvidedHandler = userApiModule.default;
+} else if (typeof userApiModule === 'function') {
+  // Handle when user defines via CJS export: "module.exports = myFunction;"
+  userProvidedHandler = userApiModule;
+}
+
 const origConfig = userApiModule.config || {};
 
 // Setting `externalResolver` to `true` prevents nextjs from throwing a warning in dev about API routes resolving
@@ -38,7 +53,7 @@ export const config = {
   },
 };
 
-export default Sentry.withSentryAPI(maybeWrappedHandler, '__ROUTE__');
+export default userProvidedHandler ? Sentry.withSentryAPI(userProvidedHandler, '__ROUTE__') : undefined;
 
 // Re-export anything exported by the page module we're wrapping. When processing this code, Rollup is smart enough to
 // not include anything whose name matchs something we've explicitly exported above.
diff --git a/packages/nextjs/test/integration/pages/api/withSentryAPI/unwrapped/cjsExport.ts b/packages/nextjs/test/integration/pages/api/withSentryAPI/unwrapped/cjsExport.ts
new file mode 100644
index 000000000000..6ae521fa5cb4
--- /dev/null
+++ b/packages/nextjs/test/integration/pages/api/withSentryAPI/unwrapped/cjsExport.ts
@@ -0,0 +1,7 @@
+import { NextApiRequest, NextApiResponse } from 'next';
+
+const handler = async (_req: NextApiRequest, res: NextApiResponse): Promise<void> => {
+  res.status(200).json({ success: true });
+};
+
+module.exports = handler;
diff --git a/packages/nextjs/test/integration/pages/api/withSentryAPI/wrapped/cjsExport.ts b/packages/nextjs/test/integration/pages/api/withSentryAPI/wrapped/cjsExport.ts
new file mode 100644
index 000000000000..6ae521fa5cb4
--- /dev/null
+++ b/packages/nextjs/test/integration/pages/api/withSentryAPI/wrapped/cjsExport.ts
@@ -0,0 +1,7 @@
+import { NextApiRequest, NextApiResponse } from 'next';
+
+const handler = async (_req: NextApiRequest, res: NextApiResponse): Promise<void> => {
+  res.status(200).json({ success: true });
+};
+
+module.exports = handler;
diff --git a/packages/nextjs/test/integration/test/server/cjsApiEndpoints.js b/packages/nextjs/test/integration/test/server/cjsApiEndpoints.js
new file mode 100644
index 000000000000..e154599fcbd7
--- /dev/null
+++ b/packages/nextjs/test/integration/test/server/cjsApiEndpoints.js
@@ -0,0 +1,55 @@
+const assert = require('assert');
+
+const { sleep } = require('../utils/common');
+const { getAsync, interceptTracingRequest } = require('../utils/server');
+
+module.exports = async ({ url: urlBase, argv }) => {
+  const unwrappedRoute = '/api/withSentryAPI/unwrapped/cjsExport';
+  const interceptedUnwrappedRequest = interceptTracingRequest(
+    {
+      contexts: {
+        trace: {
+          op: 'http.server',
+          status: 'ok',
+          tags: { 'http.status_code': '200' },
+        },
+      },
+      transaction: `GET ${unwrappedRoute}`,
+      type: 'transaction',
+      request: {
+        url: `${urlBase}${unwrappedRoute}`,
+      },
+    },
+    argv,
+    'unwrapped CJS route',
+  );
+  const responseUnwrapped = await getAsync(`${urlBase}${unwrappedRoute}`);
+  assert.equal(responseUnwrapped, '{"success":true}');
+
+  const wrappedRoute = '/api/withSentryAPI/wrapped/cjsExport';
+  const interceptedWrappedRequest = interceptTracingRequest(
+    {
+      contexts: {
+        trace: {
+          op: 'http.server',
+          status: 'ok',
+          tags: { 'http.status_code': '200' },
+        },
+      },
+      transaction: `GET ${wrappedRoute}`,
+      type: 'transaction',
+      request: {
+        url: `${urlBase}${wrappedRoute}`,
+      },
+    },
+    argv,
+    'wrapped CJS route',
+  );
+  const responseWrapped = await getAsync(`${urlBase}${wrappedRoute}`);
+  assert.equal(responseWrapped, '{"success":true}');
+
+  await sleep(250);
+
+  assert.ok(interceptedUnwrappedRequest.isDone(), 'Did not intercept unwrapped request');
+  assert.ok(interceptedWrappedRequest.isDone(), 'Did not intercept wrapped request');
+};