diff --git a/.changeset/famous-monkeys-count.md b/.changeset/famous-monkeys-count.md
new file mode 100644
index 0000000000..c5151b38c3
--- /dev/null
+++ b/.changeset/famous-monkeys-count.md
@@ -0,0 +1,5 @@
+---
+'@backstage/backend-app-api': patch
+---
+
+Add support for JWKS tokens in ExternalTokenHandler.
diff --git a/docs/auth/service-to-service-auth.md b/docs/auth/service-to-service-auth.md
index 4213f8c0f9..a728bf064b 100644
--- a/docs/auth/service-to-service-auth.md
+++ b/docs/auth/service-to-service-auth.md
@@ -80,6 +80,55 @@ header:
 Authorization: Bearer eZv5o+fW3KnR3kVabMW4ZcDNLPl8nmMW
 ```
 
+## JWKS Token Auth
+
+This access method allows for external caller token authentication using configured
+JSON Web Key Sets (JWKS). This is useful for callers that are authenticating to our
+instance of Backstage with third-party tools, such as Auth0.
+
+You can configure this access method by adding one or more entries of type `jwks`
+to the `backend.auth.externalAccess` app-config key:
+
+```yaml title="in e.g. app-config.production.yaml"
+backend:
+  auth:
+    externalAccess:
+      - type: jwks
+        options:
+          url: https://example.com/.well-known/jwks.json
+          issuers:
+            - https://example.com
+          algorithms:
+            - RS256
+          audiences:
+            - example
+          subjectPrefix: custom-prefix
+      - type: jwks
+        options:
+          url: https://another-example.com/.well-known/jwks.json
+          issuers:
+            - https://example.com
+```
+
+The URL should point at an unauthenticated endpoint that returns the JWKS.
+
+Issuers specifies the issuer(s) of the JWT that the authenticating app will accept.
+Passed JWTs must have an `iss` claim which matches one of the specified issuers.
+
+Algorithms specifies the algorithm(s) that are used to verify the JWT. The passed JWTs
+must have been signed using one of the listed algorithms.
+
+Audiences specify the intended audience(s) of the JWT. The passed JWTs must have an "aud"
+claim that matches one of the audiences specified, or have no audience specified.
+
+For additional details regarding the JWKS configuration, please consult your authentication
+provider's documentation.
+
+The subject returned from the token verification will become part of the
+credentials object that the request recipient plugins get. All subjects will have the prefix
+`external:`, but you can also provide a custom subjectPrefix which will get appended before the
+subject returned from your JWKS service (ex. `external:custom-prefix:sub`).
+
 ## Legacy Tokens
 
 Plugins and backends that are _not_ on the new backend system use a legacy token
diff --git a/packages/backend-app-api/config.d.ts b/packages/backend-app-api/config.d.ts
index f84493828a..5517af4f98 100644
--- a/packages/backend-app-api/config.d.ts
+++ b/packages/backend-app-api/config.d.ts
@@ -131,6 +131,47 @@ export interface Config {
               subject: string;
             };
           }
+        | {
+            /**
+             * This access method consists of a JWKS endpoint that can be used to
+             * verify JWT tokens.
+             *
+             * Callers generate JWT tokens via 3rd party tooling
+             * and pass them in the Authorization header:
+             *
+             * ```
+             * Authorization: Bearer eZv5o+fW3KnR3kVabMW4ZcDNLPl8nmMW
+             * ```
+             */
+            type: 'jwks';
+            options: {
+              /**
+               * Sets the algorithms that should be used to verify the JWT tokens.
+               * The passed JWTs must have been signed using one of the listed algorithms.
+               */
+              algorithms?: string[];
+              /**
+               * Sets the issuers that should be used to verify the JWT tokens.
+               * Passed JWTs must have an `iss` claim which matches one of the specified issuers.
+               */
+              issuers?: string[];
+              /**
+               * Sets the audiences that should be used to verify the JWT tokens.
+               * The passed JWTs must have an "aud" claim that matches one of the audiences specified,
+               * or have no audience specified.
+               */
+              audiences?: string[];
+              /**
+               * Sets an optional subject prefix. Passes the subject to called plugins.
+               * Useful for debugging and tracking purposes.
+               */
+              subjectPrefix?: string;
+              /**
+               * Sets the URL containing the JWKS endpoint.
+               */
+              url: string;
+            };
+          }
       >;
     };
   };
diff --git a/packages/backend-app-api/src/services/implementations/auth/external/ExternalTokenHandler.ts b/packages/backend-app-api/src/services/implementations/auth/external/ExternalTokenHandler.ts
index 588a1f1794..79ad8dd3c4 100644
--- a/packages/backend-app-api/src/services/implementations/auth/external/ExternalTokenHandler.ts
+++ b/packages/backend-app-api/src/services/implementations/auth/external/ExternalTokenHandler.ts
@@ -21,6 +21,7 @@ import {
 import { LegacyTokenHandler } from './legacy';
 import { StaticTokenHandler } from './static';
 import { TokenHandler } from './types';
+import { JWKSHandler } from './jwks';
 
 const NEW_CONFIG_KEY = 'backend.auth.externalAccess';
 const OLD_CONFIG_KEY = 'backend.auth.keys';
@@ -40,9 +41,11 @@ export class ExternalTokenHandler {
 
     const staticHandler = new StaticTokenHandler();
     const legacyHandler = new LegacyTokenHandler();
+    const jwksHandler = new JWKSHandler();
     const handlers: Record<string, TokenHandler> = {
       static: staticHandler,
       legacy: legacyHandler,
+      jwks: jwksHandler,
     };
 
     // Load the new-style handlers
diff --git a/packages/backend-app-api/src/services/implementations/auth/external/jwks.test.ts b/packages/backend-app-api/src/services/implementations/auth/external/jwks.test.ts
new file mode 100644
index 0000000000..4cbdcb1cb0
--- /dev/null
+++ b/packages/backend-app-api/src/services/implementations/auth/external/jwks.test.ts
@@ -0,0 +1,223 @@
+/*
+ * Copyright 2024 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 { setupRequestMockHandlers } from '@backstage/backend-test-utils';
+import { ConfigReader } from '@backstage/config';
+import { SignJWT, exportJWK, generateKeyPair } from 'jose';
+import { rest } from 'msw';
+import { setupServer } from 'msw/node';
+import { v4 as uuid } from 'uuid';
+import { JWKSHandler } from './jwks';
+
+interface AnyJWK extends Record<string, string> {
+  use: 'sig';
+  alg: string;
+  kid: string;
+  kty: string;
+}
+// Simplified copy of TokenFactory in @backstage/plugin-auth-backend
+class FakeTokenFactory {
+  private readonly keys = new Array<AnyJWK>();
+
+  constructor(
+    private readonly options: {
+      issuer: string;
+      keyDurationSeconds: number;
+    },
+  ) {}
+
+  async issueToken(params: {
+    claims: {
+      sub: string;
+      ent?: string[];
+    };
+  }): Promise<string> {
+    const pair = await generateKeyPair('RS256');
+    const publicKey = await exportJWK(pair.publicKey);
+    const kid = uuid();
+    publicKey.kid = kid;
+    this.keys.push(publicKey as AnyJWK);
+
+    const iss = this.options.issuer;
+    const sub = params.claims.sub;
+    const ent = params.claims.ent;
+    const aud = 'backstage';
+    const iat = Math.floor(Date.now() / 1000);
+    const exp = iat + this.options.keyDurationSeconds;
+
+    return new SignJWT({ iss, sub, aud, iat, exp, ent, kid })
+      .setProtectedHeader({ alg: 'RS256', ent: ent, kid: kid })
+      .setIssuer(iss)
+      .setAudience(aud)
+      .setSubject(sub)
+      .setIssuedAt(iat)
+      .setExpirationTime(exp)
+      .sign(pair.privateKey);
+  }
+
+  async listPublicKeys(): Promise<{ keys: AnyJWK[] }> {
+    return { keys: this.keys };
+  }
+}
+
+const server = setupServer();
+const mockBaseUrl = 'http://backstage:9191/i-am-a-mock-base';
+
+describe('JWKSHandler', () => {
+  let factory: FakeTokenFactory;
+  let mockSubject: string;
+  const keyDurationSeconds = 5;
+
+  setupRequestMockHandlers(server);
+
+  beforeEach(() => {
+    mockSubject = 'test_subject';
+
+    factory = new FakeTokenFactory({
+      issuer: mockBaseUrl,
+      keyDurationSeconds,
+    });
+
+    server.use(
+      rest.get(`${mockBaseUrl}/.well-known/jwks.json`, async (_, res, ctx) => {
+        const keys = await factory.listPublicKeys();
+        return res(ctx.json(keys));
+      }),
+    );
+  });
+
+  it('verifies token with valid entry', async () => {
+    const validEntry = {
+      url: `${mockBaseUrl}/.well-known/jwks.json`,
+      algorithms: ['RS256'],
+      issuers: [mockBaseUrl],
+      audiences: ['backstage'],
+    };
+    const jwksHandler = new JWKSHandler();
+
+    jwksHandler.add(new ConfigReader(validEntry));
+
+    const token = await factory.issueToken({
+      claims: { sub: mockSubject },
+    });
+
+    const result = await jwksHandler.verifyToken(token);
+
+    expect(result).toEqual({ subject: `external:${mockSubject}` });
+  });
+
+  it('skips invalid entry and continues verification', async () => {
+    const invalidEntry = {
+      url: `${mockBaseUrl}/.well-known/jwks.json`,
+      algorithms: ['RS256'],
+      issuers: ['fakeIssuer'],
+      audiences: ['fakeAud'],
+    };
+
+    const validEntry = {
+      url: `${mockBaseUrl}/.well-known/jwks.json`,
+      algorithms: ['RS256'],
+      issuers: ['multiple-issuers', mockBaseUrl],
+      audiences: ['multiple-audiences', 'backstage'],
+    };
+    const jwksHandler = new JWKSHandler();
+
+    jwksHandler.add(new ConfigReader(invalidEntry));
+    jwksHandler.add(new ConfigReader(validEntry));
+
+    const token = await factory.issueToken({
+      claims: { sub: mockSubject },
+    });
+
+    const result = await jwksHandler.verifyToken(token);
+
+    expect(result).toEqual({ subject: `external:${mockSubject}` });
+  });
+
+  it('returns undefined if no valid entry found', async () => {
+    const invalidEntry1 = {
+      url: `${mockBaseUrl}/.well-known/jwks.json`,
+      algorithms: ['RS256'],
+      issuers: [mockBaseUrl],
+      audiences: [],
+    };
+
+    const invalidEntry2 = {
+      url: `${mockBaseUrl}/.well-known/jwks.json`,
+      algorithms: ['HS256'],
+      issuers: [],
+      audiences: ['backstage'],
+    };
+    const jwksHandler = new JWKSHandler();
+
+    jwksHandler.add(new ConfigReader(invalidEntry1));
+    jwksHandler.add(new ConfigReader(invalidEntry2));
+
+    const token = await factory.issueToken({
+      claims: { sub: mockSubject },
+    });
+
+    const result = await jwksHandler.verifyToken(token);
+
+    expect(result).toBeUndefined();
+  });
+
+  it('rejects bad config', () => {
+    const jwksHandler = new JWKSHandler();
+
+    expect(() => {
+      jwksHandler.add(
+        new ConfigReader({
+          url: 'https://exampl e.com/jwks',
+        }),
+      );
+    }).toThrow('Invalid URL');
+    expect(() => {
+      jwksHandler.add(
+        new ConfigReader({
+          url: 'https://example.com/jwks\n',
+        }),
+      );
+    }).toThrow('Illegal URL, must be a set of non-space characters');
+  });
+
+  it('gracefully handles no added tokens', async () => {
+    const handler = new JWKSHandler();
+    await expect(handler.verifyToken('ghi')).resolves.toBeUndefined();
+  });
+
+  it('uses custom subject prefix if provided', async () => {
+    const validEntry = {
+      url: `${mockBaseUrl}/.well-known/jwks.json`,
+      algorithms: ['RS256'],
+      issuers: [mockBaseUrl],
+      audiences: ['backstage'],
+      subjectPrefix: 'custom-prefix',
+    };
+    const jwksHandler = new JWKSHandler();
+
+    jwksHandler.add(new ConfigReader(validEntry));
+
+    const token = await factory.issueToken({
+      claims: { sub: mockSubject },
+    });
+
+    const result = await jwksHandler.verifyToken(token);
+
+    expect(result).toEqual({
+      subject: `external:${validEntry.subjectPrefix}:${mockSubject}`,
+    });
+  });
+});
diff --git a/packages/backend-app-api/src/services/implementations/auth/external/jwks.ts b/packages/backend-app-api/src/services/implementations/auth/external/jwks.ts
new file mode 100644
index 0000000000..ea62b3880c
--- /dev/null
+++ b/packages/backend-app-api/src/services/implementations/auth/external/jwks.ts
@@ -0,0 +1,82 @@
+/*
+ * Copyright 2024 The Backstage Authors
+ *
+ * Licensed under the Apache License, Version 2.0 (the "License");
+ * you may not use this file except in compliance with the License.
+ * You may obtain a copy of the License at
+ *
+ *     http://www.apache.org/licenses/LICENSE-2.0
+ *
+ * Unless required by applicable law or agreed to in writing, software
+ * distributed under the License is distributed on an "AS IS" BASIS,
+ * WITHOUT WARRANTIES OR CONDITIONS OF ANY KIND, either express or implied.
+ * See the License for the specific language governing permissions and
+ * limitations under the License.
+ */
+
+import { jwtVerify, createRemoteJWKSet, JWTVerifyGetKey } from 'jose';
+import { Config } from '@backstage/config';
+import { TokenHandler } from './types';
+
+/**
+ * Handles `type: jwks` access.
+ *
+ * @internal
+ */
+export class JWKSHandler implements TokenHandler {
+  #entries: Array<{
+    algorithms?: string[];
+    audiences?: string[];
+    issuers?: string[];
+    subjectPrefix?: string;
+    url: URL;
+    jwks: JWTVerifyGetKey;
+  }> = [];
+
+  add(options: Config) {
+    const algorithms = options.getOptionalStringArray('algorithms');
+    const issuers = options.getOptionalStringArray('issuers');
+    const audiences = options.getOptionalStringArray('audiences');
+    const subjectPrefix = options.getOptionalString('subjectPrefix');
+    const url = new URL(options.getString('url'));
+    const jwks = createRemoteJWKSet(url);
+
+    if (!options.getString('url').match(/^\S+$/)) {
+      throw new Error('Illegal URL, must be a set of non-space characters');
+    }
+
+    this.#entries.push({
+      algorithms,
+      audiences,
+      issuers,
+      jwks,
+      subjectPrefix,
+      url,
+    });
+  }
+
+  async verifyToken(token: string) {
+    for (const entry of this.#entries) {
+      try {
+        const {
+          payload: { sub },
+        } = await jwtVerify(token, entry.jwks, {
+          algorithms: entry.algorithms,
+          issuer: entry.issuers,
+          audience: entry.audiences,
+        });
+
+        if (sub) {
+          if (entry.subjectPrefix) {
+            return { subject: `external:${entry.subjectPrefix}:${sub}` };
+          }
+
+          return { subject: `external:${sub}` };
+        }
+      } catch {
+        continue;
+      }
+    }
+    return undefined;
+  }
+}