diff --git a/.changeset/rate-limit-ipv6-key-generator.md b/.changeset/rate-limit-ipv6-key-generator.md
new file mode 100644
index 0000000000..21fd7c3b34
--- /dev/null
+++ b/.changeset/rate-limit-ipv6-key-generator.md
@@ -0,0 +1,5 @@
+---
+'@backstage/backend-defaults': patch
+---
+
+Fixed the built-in rate limiter throwing a validation error and refusing to start when `backend.rateLimit` is enabled. Requests are now keyed using the address normalization helper from `express-rate-limit`, which is required by newer versions of that library and ensures IPv6 clients are grouped by their address block rather than by individual address.
diff --git a/packages/backend-defaults/src/lib/rateLimitMiddleware.test.ts b/packages/backend-defaults/src/lib/rateLimitMiddleware.test.ts
new file mode 100644
index 0000000000..38a989b805
--- /dev/null
+++ b/packages/backend-defaults/src/lib/rateLimitMiddleware.test.ts
@@ -0,0 +1,93 @@
+/*
+ * Copyright 2025 The Backstage Authors
+ *
+ * Licensed under the Apache License, Version 2.0 (the "License");
+ * you may not use this file except in compliance with the License.
+ * You may obtain a copy of the License at
+ *
+ *     http://www.apache.org/licenses/LICENSE-2.0
+ *
+ * Unless required by applicable law or agreed to in writing, software
+ * distributed under the License is distributed on an "AS IS" BASIS,
+ * WITHOUT WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied.
+ * See the License for the specific language governing permissions and
+ * limitations under the License.
+ */
+
+import { ConfigReader } from '@backstage/config';
+import express from 'express';
+import request from 'supertest';
+import { rateLimitMiddleware } from './rateLimitMiddleware';
+
+function createApp(config: ConfigReader) {
+  const app = express();
+  // Mimic a backend running behind a proxy so that the X-Forwarded-For header
+  // is used to populate `req.ip`, allowing us to exercise IPv6 client handling.
+  app.set('trust proxy', true);
+  app.use(rateLimitMiddleware({ config }));
+  app.get('/', (_req, res) => {
+    res.status(200).send('ok');
+  });
+  return app;
+}
+
+describe('rateLimitMiddleware', () => {
+  it('limits requests per client and handles IPv6 addresses without key generator validation errors', async () => {
+    const errorSpy = jest.spyOn(console, 'error').mockImplementation(() => {});
+    const warnSpy = jest.spyOn(console, 'warn').mockImplementation(() => {});
+
+    const app = createApp(
+      new ConfigReader({ incomingRequestLimit: 2, ipAllowList: [] }),
+    );
+    const agent = request(app);
+    const ipv6 = '2001:db8::1';
+
+    const first = await agent.get('/').set('X-Forwarded-For', ipv6);
+    const second = await agent.get('/').set('X-Forwarded-For', ipv6);
+    const third = await agent.get('/').set('X-Forwarded-For', ipv6);
+
+    expect(first.status).toBe(200);
+    expect(second.status).toBe(200);
+    expect(third.status).toBe(429);
+    expect(third.body).toEqual({
+      error: {
+        name: 'Error',
+        message: 'Too many requests, please try again later',
+      },
+      response: { statusCode: 429 },
+    });
+
+    // express-rate-limit 8.x rejects key generators that reference `req.ip`
+    // without using its `ipKeyGenerator` helper, reporting an ERR_ERL_KEY_GEN_IPV6
+    // validation error. Make sure our key generator does not trip that check.
+    const logs = [...errorSpy.mock.calls, ...warnSpy.mock.calls]
+      .flat()
+      .map(arg =>
+        arg instanceof Error
+          ? `${arg.message} ${(arg as { code?: string }).code ?? ''}`
+          : String(arg),
+      )
+      .join('\n');
+    expect(logs).not.toMatch(/IPV6|ipKeyGenerator/i);
+
+    errorSpy.mockRestore();
+    warnSpy.mockRestore();
+  });
+
+  it('does not rate limit addresses on the allow list', async () => {
+    const app = createApp(
+      new ConfigReader({
+        incomingRequestLimit: 1,
+        ipAllowList: ['2001:db8::5'],
+      }),
+    );
+    const agent = request(app);
+
+    for (let i = 0; i < 3; i++) {
+      const response = await agent
+        .get('/')
+        .set('X-Forwarded-For', '2001:db8::5');
+      expect(response.status).toBe(200);
+    }
+  });
+});
diff --git a/packages/backend-defaults/src/lib/rateLimitMiddleware.ts b/packages/backend-defaults/src/lib/rateLimitMiddleware.ts
index 57163b5908..74179ff232 100644
--- a/packages/backend-defaults/src/lib/rateLimitMiddleware.ts
+++ b/packages/backend-defaults/src/lib/rateLimitMiddleware.ts
@@ -14,7 +14,7 @@
  * limitations under the License.
  */
 import { RequestHandler } from 'express';
-import { rateLimit, Store } from 'express-rate-limit';
+import { ipKeyGenerator, rateLimit, Store } from 'express-rate-limit';
 import { Config, readDurationFromConfig } from '@backstage/config';
 import { durationToMilliseconds } from '@backstage/types';
 
@@ -59,10 +59,13 @@ export const rateLimitMiddleware = (options: {
     skipFailedRequests,
     passOnStoreError: passOnStoreError,
     keyGenerator(req, _res): string {
-      if (!req.ip) {
-        return req.socket.remoteAddress!;
-      }
-      return req.ip;
+      // `ipKeyGenerator` normalizes the address before it is used as a rate
+      // limiting key. This is required by express-rate-limit 8.x, which rejects
+      // key generators that reference `req.ip` directly, as a naive IPv6 key
+      // would let clients trivially bypass the limit by rotating addresses
+      // within their allotted block.
+      const ip = req.ip ?? req.socket.remoteAddress;
+      return ip ? ipKeyGenerator(ip) : '';
     },
     skip: (req, _res) => {
       return (