diff --git a/packages/firestore/src/api/database.ts b/packages/firestore/src/api/database.ts
index a2feb19507f..f894ddce03e 100644
--- a/packages/firestore/src/api/database.ts
+++ b/packages/firestore/src/api/database.ts
@@ -302,6 +302,7 @@ export function configureFirestore(firestore: Firestore): void {
     firestore._databaseId,
     firestore._app?.options.appId || '',
     firestore._persistenceKey,
+    firestore._app?.options.apiKey,
     settings
   );
   if (!firestore._componentsProvider) {
diff --git a/packages/firestore/src/core/database_info.ts b/packages/firestore/src/core/database_info.ts
index a057516763f..ec75ba2486f 100644
--- a/packages/firestore/src/core/database_info.ts
+++ b/packages/firestore/src/core/database_info.ts
@@ -49,7 +49,8 @@ export class DatabaseInfo {
     readonly autoDetectLongPolling: boolean,
     readonly longPollingOptions: ExperimentalLongPollingOptions,
     readonly useFetchStreams: boolean,
-    readonly isUsingEmulator: boolean
+    readonly isUsingEmulator: boolean,
+    readonly apiKey: string | undefined
   ) {}
 }
 
diff --git a/packages/firestore/src/core/firestore_client.ts b/packages/firestore/src/core/firestore_client.ts
index 009e7b2aba2..124ab4eaa44 100644
--- a/packages/firestore/src/core/firestore_client.ts
+++ b/packages/firestore/src/core/firestore_client.ts
@@ -146,7 +146,11 @@ export class FirestoreClient {
      * an async I/O to complete).
      */
     public asyncQueue: AsyncQueue,
-    private databaseInfo: DatabaseInfo,
+    /**
+     * @internal
+     * Exposed for testing
+     */
+    public _databaseInfo: DatabaseInfo,
     componentProvider?: {
       _offline: OfflineComponentProvider;
       _online: OnlineComponentProvider;
@@ -167,7 +171,7 @@ export class FirestoreClient {
   get configuration(): ComponentConfiguration {
     return {
       asyncQueue: this.asyncQueue,
-      databaseInfo: this.databaseInfo,
+      databaseInfo: this._databaseInfo,
       clientId: this.clientId,
       authCredentials: this.authCredentials,
       appCheckCredentials: this.appCheckCredentials,
diff --git a/packages/firestore/src/lite-api/components.ts b/packages/firestore/src/lite-api/components.ts
index 52c3b3729ee..d956fcd31f5 100644
--- a/packages/firestore/src/lite-api/components.ts
+++ b/packages/firestore/src/lite-api/components.ts
@@ -75,6 +75,7 @@ export function getDatastore(firestore: FirestoreService): Datastore {
       firestore._databaseId,
       firestore.app.options.appId || '',
       firestore._persistenceKey,
+      firestore.app.options.apiKey,
       firestore._freezeSettings()
     );
     const connection = newConnection(databaseInfo);
@@ -108,6 +109,7 @@ export function makeDatabaseInfo(
   databaseId: DatabaseId,
   appId: string,
   persistenceKey: string,
+  apiKey: string | undefined,
   settings: FirestoreSettingsImpl
 ): DatabaseInfo {
   return new DatabaseInfo(
@@ -120,6 +122,7 @@ export function makeDatabaseInfo(
     settings.experimentalAutoDetectLongPolling,
     cloneLongPollingOptions(settings.experimentalLongPollingOptions),
     settings.useFetchStreams,
-    settings.isUsingEmulator
+    settings.isUsingEmulator,
+    apiKey
   );
 }
diff --git a/packages/firestore/src/platform/node/grpc_connection.ts b/packages/firestore/src/platform/node/grpc_connection.ts
index d50a3149416..79ccb3ddf3c 100644
--- a/packages/firestore/src/platform/node/grpc_connection.ts
+++ b/packages/firestore/src/platform/node/grpc_connection.ts
@@ -44,7 +44,8 @@ function createMetadata(
   databasePath: string,
   authToken: Token | null,
   appCheckToken: Token | null,
-  appId: string
+  appId: string,
+  apiKey: string | undefined
 ): grpc.Metadata {
   hardAssert(
     authToken === null || authToken.type === 'OAuth',
@@ -69,6 +70,9 @@ function createMetadata(
   // 11 from Google3.
   metadata.set('Google-Cloud-Resource-Prefix', databasePath);
   metadata.set('x-goog-request-params', databasePath);
+  if (apiKey) {
+    metadata.set('X-Goog-Api-Key', apiKey);
+  }
   return metadata;
 }
 
@@ -100,7 +104,8 @@ export class GrpcConnection implements Connection {
     this.databasePath = `projects/${databaseInfo.databaseId.projectId}/databases/${databaseInfo.databaseId.database}`;
   }
 
-  private ensureActiveStub(): GeneratedGrpcStub {
+  /** made protected for testing */
+  protected ensureActiveStub(): GeneratedGrpcStub {
     if (!this.cachedStub) {
       logDebug(LOG_TAG, 'Creating Firestore stub.');
       const credentials = this.databaseInfo.ssl
@@ -127,7 +132,8 @@ export class GrpcConnection implements Connection {
       this.databasePath,
       authToken,
       appCheckToken,
-      this.databaseInfo.appId
+      this.databaseInfo.appId,
+      this.databaseInfo.apiKey
     );
     const jsonRequest = { database: this.databasePath, ...request };
 
@@ -187,7 +193,8 @@ export class GrpcConnection implements Connection {
       this.databasePath,
       authToken,
       appCheckToken,
-      this.databaseInfo.appId
+      this.databaseInfo.appId,
+      this.databaseInfo.apiKey
     );
     const jsonRequest = { ...request, database: this.databasePath };
     const stream = stub[rpcName](jsonRequest, metadata);
@@ -239,7 +246,8 @@ export class GrpcConnection implements Connection {
       this.databasePath,
       authToken,
       appCheckToken,
-      this.databaseInfo.appId
+      this.databaseInfo.appId,
+      this.databaseInfo.apiKey
     );
     const grpcStream = stub[rpcName](metadata);
 
diff --git a/packages/firestore/src/remote/rest_connection.ts b/packages/firestore/src/remote/rest_connection.ts
index 7469d8f45ff..d9446a733e5 100644
--- a/packages/firestore/src/remote/rest_connection.ts
+++ b/packages/firestore/src/remote/rest_connection.ts
@@ -64,6 +64,7 @@ export abstract class RestConnection implements Connection {
   protected readonly baseUrl: string;
   private readonly databasePath: string;
   private readonly requestParams: string;
+  private readonly apiKey: string | undefined;
 
   get shouldResourcePathBeIncludedInRequest(): boolean {
     // Both `invokeRPC()` and `invokeStreamingRPC()` use their `path` arguments to determine
@@ -82,6 +83,7 @@ export abstract class RestConnection implements Connection {
       this.databaseId.database === DEFAULT_DATABASE_NAME
         ? `project_id=${projectId}`
         : `project_id=${projectId}&database_id=${databaseId}`;
+    this.apiKey = databaseInfo.apiKey;
   }
 
   invokeRPC<Req, Resp>(
@@ -194,13 +196,17 @@ export abstract class RestConnection implements Connection {
     _forwardCredentials: boolean
   ): Promise<Resp>;
 
-  private makeUrl(rpcName: string, path: string): string {
+  protected makeUrl(rpcName: string, path: string): string {
     const urlRpcName = RPC_NAME_URL_MAPPING[rpcName];
     debugAssert(
       urlRpcName !== undefined,
       'Unknown REST mapping for: ' + rpcName
     );
-    return `${this.baseUrl}/${RPC_URL_VERSION}/${path}:${urlRpcName}`;
+    let url = `${this.baseUrl}/${RPC_URL_VERSION}/${path}:${urlRpcName}`;
+    if (this.apiKey) {
+      url = `${url}?key=${encodeURIComponent(this.apiKey)}`;
+    }
+    return url;
   }
 
   /**
diff --git a/packages/firestore/test/integration/api/provider.test.ts b/packages/firestore/test/integration/api/provider.test.ts
index cc7888a5385..95d825c2a9e 100644
--- a/packages/firestore/test/integration/api/provider.test.ts
+++ b/packages/firestore/test/integration/api/provider.test.ts
@@ -29,7 +29,8 @@ import {
   enableIndexedDbPersistence,
   setDoc,
   memoryLocalCache,
-  getDocFromCache
+  getDocFromCache,
+  ensureFirestoreConfigured
 } from '../util/firebase_export';
 import { DEFAULT_SETTINGS } from '../util/settings';
 
@@ -200,4 +201,17 @@ describe('Firestore Provider', () => {
 
     return terminate(firestore).then(() => terminate(firestore));
   });
+
+  it('passes API key to database info', () => {
+    const app = initializeApp(
+      { apiKey: 'fake-api-key-x', projectId: 'test-project' },
+      'test-app-getFirestore-x'
+    );
+    const fs = getFirestore(app);
+    ensureFirestoreConfigured(fs);
+
+    expect(fs._firestoreClient?._databaseInfo.apiKey).to.equal(
+      'fake-api-key-x'
+    );
+  });
 });
diff --git a/packages/firestore/test/integration/util/internal_helpers.ts b/packages/firestore/test/integration/util/internal_helpers.ts
index e5e64b5fbf4..b196599f408 100644
--- a/packages/firestore/test/integration/util/internal_helpers.ts
+++ b/packages/firestore/test/integration/util/internal_helpers.ts
@@ -62,7 +62,8 @@ export function getDefaultDatabaseInfo(): DatabaseInfo {
       DEFAULT_SETTINGS.experimentalLongPollingOptions ?? {}
     ),
     /*use FetchStreams= */ false,
-    /*isUsingEmulator=*/ false
+    /*isUsingEmulator=*/ false,
+    undefined
   );
 }
 
diff --git a/packages/firestore/test/unit/remote/fetch_connection.test.ts b/packages/firestore/test/unit/remote/fetch_connection.test.ts
index 5a9aa67436f..4de0ba5a722 100644
--- a/packages/firestore/test/unit/remote/fetch_connection.test.ts
+++ b/packages/firestore/test/unit/remote/fetch_connection.test.ts
@@ -43,6 +43,7 @@ describe('Fetch Connection', () => {
         DatabaseId.empty(),
         '',
         '',
+        '',
         new FirestoreSettingsImpl({
           host: 'abc.cloudworkstations.dev'
         })
diff --git a/packages/firestore/test/unit/remote/grpc_connection.test.ts b/packages/firestore/test/unit/remote/grpc_connection.test.ts
new file mode 100644
index 00000000000..8364cbbd5e6
--- /dev/null
+++ b/packages/firestore/test/unit/remote/grpc_connection.test.ts
@@ -0,0 +1,81 @@
+/**
+ * @license
+ * Copyright 2025 Google LLC
+ *
+ * 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 { Metadata } from '@grpc/grpc-js';
+import { expect } from 'chai';
+
+import { DatabaseId, DatabaseInfo } from '../../../src/core/database_info';
+import { ResourcePath } from '../../../src/model/path';
+import { GrpcConnection } from '../../../src/platform/node/grpc_connection';
+
+export class TestGrpcConnection extends GrpcConnection {
+  mockStub = {
+    lastMetadata: null,
+    mockRpc(
+      req: unknown,
+      metadata: Metadata,
+      callback: (err: unknown, resp: unknown) => void
+    ) {
+      this.lastMetadata = metadata;
+      callback(null, null);
+    }
+  } as {
+    lastMetadata: null | Metadata;
+    [index: string]: unknown;
+  };
+
+  protected ensureActiveStub(): unknown {
+    return this.mockStub;
+  }
+}
+
+describe('GrpcConnection', () => {
+  const testDatabaseInfo = new DatabaseInfo(
+    new DatabaseId('testproject'),
+    'test-app-id',
+    'persistenceKey',
+    'example.com',
+    /*ssl=*/ false,
+    /*forceLongPolling=*/ false,
+    /*autoDetectLongPolling=*/ false,
+    /*longPollingOptions=*/ {},
+    /*useFetchStreams=*/ false,
+    /*isUsingEmulator=*/ false,
+    'grpc-connection-test-api-key'
+  );
+  const connection = new TestGrpcConnection(
+    { google: { firestore: { v1: {} } } },
+    testDatabaseInfo
+  );
+
+  it('Passes the API Key from DatabaseInfo to the grpc stub', async () => {
+    const request = {
+      database: 'projects/testproject/databases/(default)',
+      writes: []
+    };
+    await connection.invokeRPC(
+      'mockRpc',
+      ResourcePath.emptyPath(),
+      request,
+      null,
+      null
+    );
+    expect(
+      connection.mockStub.lastMetadata?.get('x-goog-api-key')
+    ).to.deep.equal(['grpc-connection-test-api-key']);
+  });
+});
diff --git a/packages/firestore/test/unit/remote/rest_connection.test.ts b/packages/firestore/test/unit/remote/rest_connection.test.ts
index 100b8b8368e..3501a910f66 100644
--- a/packages/firestore/test/unit/remote/rest_connection.test.ts
+++ b/packages/firestore/test/unit/remote/rest_connection.test.ts
@@ -68,7 +68,8 @@ describe('RestConnection', () => {
     /*autoDetectLongPolling=*/ false,
     /*longPollingOptions=*/ {},
     /*useFetchStreams=*/ false,
-    /*isUsingEmulator=*/ false
+    /*isUsingEmulator=*/ false,
+    'rest-connection-test-api-key'
   );
   const connection = new TestRestConnection(testDatabaseInfo);
 
@@ -83,7 +84,7 @@ describe('RestConnection', () => {
       null
     );
     expect(connection.lastUrl).to.equal(
-      'http://example.com/v1/projects/testproject/databases/(default)/documents:commit'
+      'http://example.com/v1/projects/testproject/databases/(default)/documents:commit?key=rest-connection-test-api-key'
     );
   });
 
diff --git a/packages/firestore/test/unit/specs/spec_test_runner.ts b/packages/firestore/test/unit/specs/spec_test_runner.ts
index 51d2229b8a1..50806cb2a48 100644
--- a/packages/firestore/test/unit/specs/spec_test_runner.ts
+++ b/packages/firestore/test/unit/specs/spec_test_runner.ts
@@ -283,7 +283,8 @@ abstract class TestRunner {
       /*autoDetectLongPolling=*/ false,
       /*longPollingOptions=*/ {},
       /*useFetchStreams=*/ false,
-      /*isUsingEmulator=*/ false
+      /*isUsingEmulator=*/ false,
+      'test-api-key'
     );
 
     // TODO(mrschmidt): During client startup in `firestore_client`, we block