diff --git a/x-pack/plugins/fleet/server/services/api_keys/enrollment_api_key.ts b/x-pack/plugins/fleet/server/services/api_keys/enrollment_api_key.ts
index f0991ab01a6ed..511a0abecbc18 100644
--- a/x-pack/plugins/fleet/server/services/api_keys/enrollment_api_key.ts
+++ b/x-pack/plugins/fleet/server/services/api_keys/enrollment_api_key.ts
@@ -14,6 +14,7 @@ import type { SavedObjectsClientContract, ElasticsearchClient } from 'src/core/s
 import { esKuery } from '../../../../../../src/plugins/data/server';
 import type { ESSearchResponse as SearchResponse } from '../../../../../../typings/elasticsearch';
 import type { EnrollmentAPIKey, FleetServerEnrollmentAPIKey } from '../../types';
+import { IngestManagerError } from '../../errors';
 import { ENROLLMENT_API_KEYS_INDEX } from '../../constants';
 import { agentPolicyService } from '../agent_policy';
 import { escapeSearchQueryPhrase } from '../saved_object';
@@ -28,10 +29,13 @@ export async function listEnrollmentApiKeys(
     page?: number;
     perPage?: number;
     kuery?: string;
+    query?: ReturnType<typeof esKuery['toElasticsearchQuery']>;
     showInactive?: boolean;
   }
 ): Promise<{ items: EnrollmentAPIKey[]; total: any; page: any; perPage: any }> {
   const { page = 1, perPage = 20, kuery } = options;
+  const query =
+    options.query ?? (kuery && esKuery.toElasticsearchQuery(esKuery.fromKueryExpression(kuery)));
 
   const res = await esClient.search<SearchResponse<FleetServerEnrollmentAPIKey, {}>>({
     index: ENROLLMENT_API_KEYS_INDEX,
@@ -40,9 +44,7 @@ export async function listEnrollmentApiKeys(
     sort: 'created_at:desc',
     track_total_hits: true,
     ignore_unavailable: true,
-    body: kuery
-      ? { query: esKuery.toElasticsearchQuery(esKuery.fromKueryExpression(kuery)) }
-      : undefined,
+    body: query ? { query } : undefined,
   });
 
   // @ts-expect-error @elastic/elasticsearch
@@ -159,7 +161,7 @@ export async function generateEnrollmentAPIKey(
       const { items } = await listEnrollmentApiKeys(esClient, {
         page: page++,
         perPage: 100,
-        kuery: `policy_id:"${agentPolicyId}" AND name:${providedKeyName.replace(/ /g, '\\ ')}*`,
+        query: getQueryForExistingKeyNameOnPolicy(agentPolicyId, providedKeyName),
       });
       if (items.length === 0) {
         hasMore = false;
@@ -176,7 +178,7 @@ export async function generateEnrollmentAPIKey(
         k.name?.replace(providedKeyName, '').trim().match(uuidRegex)
       )
     ) {
-      throw new Error(
+      throw new IngestManagerError(
         i18n.translate('xpack.fleet.serverError.enrollmentKeyDuplicate', {
           defaultMessage:
             'An enrollment key named {providedKeyName} already exists for agent policy {agentPolicyId}',
@@ -254,6 +256,29 @@ export async function generateEnrollmentAPIKey(
   };
 }
 
+function getQueryForExistingKeyNameOnPolicy(agentPolicyId: string, providedKeyName: string) {
+  const query = {
+    bool: {
+      filter: [
+        {
+          bool: {
+            should: [{ match_phrase: { policy_id: agentPolicyId } }],
+            minimum_should_match: 1,
+          },
+        },
+        {
+          bool: {
+            should: [{ query_string: { fields: ['name'], query: `(${providedKeyName}) *` } }],
+            minimum_should_match: 1,
+          },
+        },
+      ],
+    },
+  };
+
+  return query;
+}
+
 export async function getEnrollmentAPIKeyById(esClient: ElasticsearchClient, apiKeyId: string) {
   const res = await esClient.search<FleetServerEnrollmentAPIKey>({
     index: ENROLLMENT_API_KEYS_INDEX,
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 5f38a6e050f40..25fb71ae42807 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
@@ -103,7 +103,7 @@ export default function (providerContext: FtrProviderContext) {
           .expect(400);
       });
 
-      it('should allow to create an enrollment api key with an agent policy', async () => {
+      it('should allow to create an enrollment api key with only an agent policy', async () => {
         const { body: apiResponse } = await supertest
           .post(`/api/fleet/enrollment-api-keys`)
           .set('kbn-xsrf', 'xxx')
@@ -115,6 +115,55 @@ export default function (providerContext: FtrProviderContext) {
         expect(apiResponse.item).to.have.keys('id', 'api_key', 'api_key_id', 'name', 'policy_id');
       });
 
+      it('should allow to create an enrollment api key with agent policy and unique name', async () => {
+        const { body: noSpacesRes } = await supertest
+          .post(`/api/fleet/enrollment-api-keys`)
+          .set('kbn-xsrf', 'xxx')
+          .send({
+            policy_id: 'policy1',
+            name: 'something',
+          });
+        expect(noSpacesRes.item).to.have.keys('id', 'api_key', 'api_key_id', 'name', 'policy_id');
+
+        const { body: hasSpacesRes } = await supertest
+          .post(`/api/fleet/enrollment-api-keys`)
+          .set('kbn-xsrf', 'xxx')
+          .send({
+            policy_id: 'policy1',
+            name: 'something else',
+          });
+        expect(hasSpacesRes.item).to.have.keys('id', 'api_key', 'api_key_id', 'name', 'policy_id');
+
+        const { body: noSpacesDupe } = await supertest
+          .post(`/api/fleet/enrollment-api-keys`)
+          .set('kbn-xsrf', 'xxx')
+          .send({
+            policy_id: 'policy1',
+            name: 'something',
+          })
+          .expect(400);
+
+        expect(noSpacesDupe).to.eql({
+          statusCode: 400,
+          error: 'Bad Request',
+          message: 'An enrollment key named something already exists for agent policy policy1',
+        });
+
+        const { body: hasSpacesDupe } = await supertest
+          .post(`/api/fleet/enrollment-api-keys`)
+          .set('kbn-xsrf', 'xxx')
+          .send({
+            policy_id: 'policy1',
+            name: 'something else',
+          })
+          .expect(400);
+        expect(hasSpacesDupe).to.eql({
+          statusCode: 400,
+          error: 'Bad Request',
+          message: 'An enrollment key named something else already exists for agent policy policy1',
+        });
+      });
+
       it('should create an ES ApiKey with metadata', async () => {
         const { body: apiResponse } = await supertest
           .post(`/api/fleet/enrollment-api-keys`)