diff --git a/x-pack/plugins/fleet/public/applications/fleet/sections/agents/enrollment_token_list_page/components/new_enrollment_key_flyout.tsx b/x-pack/plugins/fleet/public/applications/fleet/sections/agents/enrollment_token_list_page/components/new_enrollment_key_flyout.tsx
index ed607e361bd6e5..d9aeba23726729 100644
--- a/x-pack/plugins/fleet/public/applications/fleet/sections/agents/enrollment_token_list_page/components/new_enrollment_key_flyout.tsx
+++ b/x-pack/plugins/fleet/public/applications/fleet/sections/agents/enrollment_token_list_page/components/new_enrollment_key_flyout.tsx
@@ -46,6 +46,9 @@ function useCreateApiKeyForm(
           policy_id: policyIdInput.value,
         }),
       });
+      if (res.error) {
+        throw res.error;
+      }
       policyIdInput.clear();
       apiKeyNameInput.clear();
       setIsLoading(false);
diff --git a/x-pack/plugins/fleet/server/errors/index.ts b/x-pack/plugins/fleet/server/errors/index.ts
index e3ca6a9b48dcfe..d6fa79a2baeba0 100644
--- a/x-pack/plugins/fleet/server/errors/index.ts
+++ b/x-pack/plugins/fleet/server/errors/index.ts
@@ -5,7 +5,11 @@
  */
 
 /* eslint-disable max-classes-per-file */
-export { defaultIngestErrorHandler, ingestErrorToResponseOptions } from './handlers';
+export {
+  defaultIngestErrorHandler,
+  ingestErrorToResponseOptions,
+  isLegacyESClientError,
+} from './handlers';
 
 export class IngestManagerError extends Error {
   constructor(message?: string) {
@@ -24,3 +28,4 @@ export class PackageUnsupportedMediaTypeError extends IngestManagerError {}
 export class PackageInvalidArchiveError extends IngestManagerError {}
 export class PackageCacheError extends IngestManagerError {}
 export class PackageOperationNotSupportedError extends IngestManagerError {}
+export class FleetAdminUserInvalidError extends IngestManagerError {}
diff --git a/x-pack/plugins/fleet/server/services/api_keys/security.ts b/x-pack/plugins/fleet/server/services/api_keys/security.ts
index dfd53d55fbbf5d..5fdf8626a9fb22 100644
--- a/x-pack/plugins/fleet/server/services/api_keys/security.ts
+++ b/x-pack/plugins/fleet/server/services/api_keys/security.ts
@@ -4,7 +4,9 @@
  * you may not use this file except in compliance with the Elastic License.
  */
 
-import { KibanaRequest, FakeRequest, SavedObjectsClientContract } from 'src/core/server';
+import type { Request } from '@hapi/hapi';
+import { KibanaRequest, SavedObjectsClientContract } from '../../../../../../src/core/server';
+import { FleetAdminUserInvalidError, isLegacyESClientError } from '../../errors';
 import { CallESAsCurrentUser } from '../../types';
 import { appContextService } from '../app_context';
 import { outputService } from '../output';
@@ -18,22 +20,38 @@ export async function createAPIKey(
   if (!adminUser) {
     throw new Error('No admin user configured');
   }
-  const request: FakeRequest = {
+  const request = KibanaRequest.from(({
+    path: '/',
+    route: { settings: {} },
+    url: { href: '/' },
+    raw: { req: { url: '/' } },
     headers: {
       authorization: `Basic ${Buffer.from(`${adminUser.username}:${adminUser.password}`).toString(
         'base64'
       )}`,
     },
-  };
+  } as unknown) as Request);
   const security = appContextService.getSecurity();
   if (!security) {
     throw new Error('Missing security plugin');
   }
 
-  return security.authc.createAPIKey(request as KibanaRequest, {
-    name,
-    role_descriptors: roleDescriptors,
-  });
+  try {
+    const key = await security.authc.createAPIKey(request, {
+      name,
+      role_descriptors: roleDescriptors,
+    });
+
+    return key;
+  } catch (err) {
+    if (isLegacyESClientError(err) && err.statusCode === 401) {
+      // Clear Fleet admin user cache as the user is probably not valid anymore
+      outputService.invalidateCache();
+      throw new FleetAdminUserInvalidError(`Fleet Admin user is invalid: ${err.message}`);
+    }
+
+    throw err;
+  }
 }
 export async function authenticate(callCluster: CallESAsCurrentUser) {
   try {
@@ -51,20 +69,36 @@ export async function invalidateAPIKey(soClient: SavedObjectsClientContract, id:
   if (!adminUser) {
     throw new Error('No admin user configured');
   }
-  const request: FakeRequest = {
+  const request = KibanaRequest.from(({
+    path: '/',
+    route: { settings: {} },
+    url: { href: '/' },
+    raw: { req: { url: '/' } },
     headers: {
       authorization: `Basic ${Buffer.from(`${adminUser.username}:${adminUser.password}`).toString(
         'base64'
       )}`,
     },
-  };
+  } as unknown) as Request);
 
   const security = appContextService.getSecurity();
   if (!security) {
     throw new Error('Missing security plugin');
   }
 
-  return security.authc.invalidateAPIKey(request as KibanaRequest, {
-    id,
-  });
+  try {
+    const res = await security.authc.invalidateAPIKey(request, {
+      id,
+    });
+
+    return res;
+  } catch (err) {
+    if (isLegacyESClientError(err) && err.statusCode === 401) {
+      // Clear Fleet admin user cache as the user is probably not valid anymore
+      outputService.invalidateCache();
+      throw new FleetAdminUserInvalidError(`Fleet Admin user is invalid: ${err.message}`);
+    }
+
+    throw err;
+  }
 }
diff --git a/x-pack/test/fleet_api_integration/apis/enrollment_api_keys/crud.ts b/x-pack/test/fleet_api_integration/apis/enrollment_api_keys/crud.ts
index 3a526fac2f08a1..dd72016476526d 100644
--- a/x-pack/test/fleet_api_integration/apis/enrollment_api_keys/crud.ts
+++ b/x-pack/test/fleet_api_integration/apis/enrollment_api_keys/crud.ts
@@ -92,12 +92,12 @@ export default function (providerContext: FtrProviderContext) {
           .expect(400);
       });
 
-      it('should not allow to create an enrollment api key for a non existing agent policy', async () => {
+      it('should return a 400 if the fleet admin user is modifed outside of Fleet', async () => {
         await supertest
           .post(`/api/fleet/enrollment-api-keys`)
           .set('kbn-xsrf', 'xxx')
           .send({
-            policy_id: 'idonotexistspolicy',
+            raoul: 'raoul',
           })
           .expect(400);
       });
@@ -161,6 +161,33 @@ export default function (providerContext: FtrProviderContext) {
           },
         });
       });
+
+      describe('It should handle error when the Fleet user is invalid', () => {
+        before(async () => {});
+        after(async () => {
+          await getService('supertest')
+            .post(`/api/fleet/agents/setup`)
+            .set('kbn-xsrf', 'xxx')
+            .send({ forceRecreate: true });
+        });
+
+        it('should not allow to create an enrollment api key if the Fleet admin user is invalid', async () => {
+          await es.security.changePassword({
+            username: 'fleet_enroll',
+            body: {
+              password: Buffer.from((Math.random() * 10000000).toString()).toString('base64'),
+            },
+          });
+          const res = await supertest
+            .post(`/api/fleet/enrollment-api-keys`)
+            .set('kbn-xsrf', 'xxx')
+            .send({
+              policy_id: 'policy1',
+            })
+            .expect(400);
+          expect(res.body.message).match(/Fleet Admin user is invalid/);
+        });
+      });
     });
   });
 }