diff --git a/packages/cli/src/services/__tests__/public-api-key.service.test.ts b/packages/cli/src/services/__tests__/public-api-key.service.test.ts
index 86db071f35..8aafb6f84b 100644
--- a/packages/cli/src/services/__tests__/public-api-key.service.test.ts
+++ b/packages/cli/src/services/__tests__/public-api-key.service.test.ts
@@ -1,5 +1,8 @@
+import { Container } from '@n8n/di';
 import { mock } from 'jest-mock-extended';
+import { DateTime } from 'luxon';
 import type { InstanceSettings } from 'n8n-core';
+import { randomString } from 'n8n-workflow';
 import type { OpenAPIV3 } from 'openapi-types';
 
 import { ApiKeyRepository } from '@/databases/repositories/api-key.repository';
@@ -143,6 +146,85 @@ describe('PublicApiKeyService', () => {
 				}),
 			);
 		});
+
+		it('should return false if expired JWT is used', async () => {
+			//Arrange
+
+			const path = '/test';
+			const method = 'GET';
+			const apiVersion = 'v1';
+
+			const publicApiKeyService = new PublicApiKeyService(
+				apiKeyRepository,
+				userRepository,
+				jwtService,
+				eventService,
+			);
+
+			const dateInThePast = DateTime.now().minus({ days: 1 }).toUnixInteger();
+
+			const owner = await createOwnerWithApiKey({
+				expiresAt: dateInThePast,
+			});
+
+			const [{ apiKey }] = owner.apiKeys;
+
+			const middleware = publicApiKeyService.getAuthMiddleware(apiVersion);
+
+			//Act
+
+			const response = await middleware(mockReqWith(apiKey, path, method), {}, securitySchema);
+
+			//Assert
+
+			expect(response).toBe(false);
+		});
+
+		it('should work with non JWT (legacy) api keys', async () => {
+			//Arrange
+
+			const path = '/test';
+			const method = 'GET';
+			const apiVersion = 'v1';
+			const legacyApiKey = `n8n_api_${randomString(10)}`;
+
+			const publicApiKeyService = new PublicApiKeyService(
+				apiKeyRepository,
+				userRepository,
+				jwtService,
+				eventService,
+			);
+
+			const owner = await createOwnerWithApiKey();
+
+			const [{ apiKey }] = owner.apiKeys;
+
+			await Container.get(ApiKeyRepository).update({ apiKey }, { apiKey: legacyApiKey });
+
+			const middleware = publicApiKeyService.getAuthMiddleware(apiVersion);
+
+			//Act
+
+			const response = await middleware(
+				mockReqWith(legacyApiKey, path, method),
+				{},
+				securitySchema,
+			);
+
+			//Assert
+
+			expect(response).toBe(true);
+			expect(eventService.emit).toHaveBeenCalledTimes(1);
+			expect(eventService.emit).toHaveBeenCalledWith(
+				'public-api-invoked',
+				expect.objectContaining({
+					userId: owner.id,
+					path,
+					method,
+					apiVersion: 'v1',
+				}),
+			);
+		});
 	});
 
 	describe('redactApiKey', () => {
diff --git a/packages/cli/src/services/public-api-key.service.ts b/packages/cli/src/services/public-api-key.service.ts
index 719f922fb2..c21129412b 100644
--- a/packages/cli/src/services/public-api-key.service.ts
+++ b/packages/cli/src/services/public-api-key.service.ts
@@ -17,6 +17,7 @@ const API_KEY_AUDIENCE = 'public-api';
 const API_KEY_ISSUER = 'n8n';
 const REDACT_API_KEY_REVEAL_COUNT = 4;
 const REDACT_API_KEY_MAX_LENGTH = 10;
+const PREFIX_LEGACY_API_KEY = 'n8n_api_';
 
 @Service()
 export class PublicApiKeyService {
@@ -107,14 +108,17 @@ export class PublicApiKeyService {
 
 			if (!user) return false;
 
-			try {
-				this.jwtService.verify(providedApiKey, {
-					issuer: API_KEY_ISSUER,
-					audience: API_KEY_AUDIENCE,
-				});
-			} catch (e) {
-				if (e instanceof TokenExpiredError) return false;
-				throw e;
+			// Legacy API keys are not JWTs and do not need to be verified.
+			if (!providedApiKey.startsWith(PREFIX_LEGACY_API_KEY)) {
+				try {
+					this.jwtService.verify(providedApiKey, {
+						issuer: API_KEY_ISSUER,
+						audience: API_KEY_AUDIENCE,
+					});
+				} catch (e) {
+					if (e instanceof TokenExpiredError) return false;
+					throw e;
+				}
 			}
 
 			this.eventService.emit('public-api-invoked', {
diff --git a/packages/cli/test/integration/shared/db/users.ts b/packages/cli/test/integration/shared/db/users.ts
index af0cf99820..be40ed7d23 100644
--- a/packages/cli/test/integration/shared/db/users.ts
+++ b/packages/cli/test/integration/shared/db/users.ts
@@ -80,23 +80,30 @@ export async function createUserWithMfaEnabled(
 	};
 }
 
-export const addApiKey = async (user: User) => {
+export const addApiKey = async (
+	user: User,
+	{ expiresAt = null }: { expiresAt?: number | null } = {},
+) => {
 	return await Container.get(PublicApiKeyService).createPublicApiKeyForUser(user, {
 		label: randomName(),
-		expiresAt: null,
+		expiresAt,
 	});
 };
 
-export async function createOwnerWithApiKey() {
+export async function createOwnerWithApiKey({
+	expiresAt = null,
+}: { expiresAt?: number | null } = {}) {
 	const owner = await createOwner();
-	const apiKey = await addApiKey(owner);
+	const apiKey = await addApiKey(owner, { expiresAt });
 	owner.apiKeys = [apiKey];
 	return owner;
 }
 
-export async function createMemberWithApiKey() {
+export async function createMemberWithApiKey({
+	expiresAt = null,
+}: { expiresAt?: number | null } = {}) {
 	const member = await createMember();
-	const apiKey = await addApiKey(member);
+	const apiKey = await addApiKey(member, { expiresAt });
 	member.apiKeys = [apiKey];
 	return member;
 }