diff --git a/packages/firestore/src/platform/browser/webchannel_connection.ts b/packages/firestore/src/platform/browser/webchannel_connection.ts
index 56f57aa9595..32673669b4d 100644
--- a/packages/firestore/src/platform/browser/webchannel_connection.ts
+++ b/packages/firestore/src/platform/browser/webchannel_connection.ts
@@ -16,7 +16,7 @@
  */
 
 import {
-  createWebChannelTransport,
+  createWebChannelTransport as internalCreateWebChannelTransport,
   ErrorCode,
   EventType,
   WebChannel,
@@ -27,7 +27,8 @@ import {
   EventTarget,
   StatEvent,
   Event,
-  Stat
+  Stat,
+  WebChannelTransport
 } from '@firebase/webchannel-wrapper/webchannel-blob';
 
 import { Token } from '../../api/credentials';
@@ -181,7 +182,7 @@ export class WebChannelConnection extends RestConnection {
       rpcName,
       '/channel'
     ];
-    const webchannelTransport = createWebChannelTransport();
+    const webchannelTransport = this.createWebChannelTransport();
     const requestStats = getStatEventTarget();
     const request: WebChannelOptions = {
       // Required for backend stickiness, routing behavior is based on this
@@ -460,4 +461,29 @@ export class WebChannelConnection extends RestConnection {
       instance => instance === webChannel
     );
   }
+
+  /**
+   * Modifies the headers for a request, adding the api key if present,
+   * and then calling super.modifyHeadersForRequest
+   */
+  protected modifyHeadersForRequest(
+    headers: StringMap,
+    authToken: Token | null,
+    appCheckToken: Token | null
+  ): void {
+    super.modifyHeadersForRequest(headers, authToken, appCheckToken);
+
+    // For web channel streams, we want to send the api key in the headers.
+    if (this.databaseInfo.apiKey) {
+      headers['x-goog-api-key'] = this.databaseInfo.apiKey;
+    }
+  }
+
+  /**
+   * Wrapped for mocking.
+   * @protected
+   */
+  protected createWebChannelTransport(): WebChannelTransport {
+    return internalCreateWebChannelTransport();
+  }
 }
diff --git a/packages/firestore/src/remote/rest_connection.ts b/packages/firestore/src/remote/rest_connection.ts
index d9446a733e5..83b0c572f9a 100644
--- a/packages/firestore/src/remote/rest_connection.ts
+++ b/packages/firestore/src/remote/rest_connection.ts
@@ -64,7 +64,6 @@ 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
@@ -72,7 +71,7 @@ export abstract class RestConnection implements Connection {
     return false;
   }
 
-  constructor(private readonly databaseInfo: DatabaseInfo) {
+  constructor(protected readonly databaseInfo: DatabaseInfo) {
     this.databaseId = databaseInfo.databaseId;
     const proto = databaseInfo.ssl ? 'https' : 'http';
     const projectId = encodeURIComponent(this.databaseId.projectId);
@@ -83,7 +82,6 @@ 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>(
@@ -203,8 +201,8 @@ export abstract class RestConnection implements Connection {
       'Unknown REST mapping for: ' + rpcName
     );
     let url = `${this.baseUrl}/${RPC_URL_VERSION}/${path}:${urlRpcName}`;
-    if (this.apiKey) {
-      url = `${url}?key=${encodeURIComponent(this.apiKey)}`;
+    if (this.databaseInfo.apiKey) {
+      url = `${url}?key=${encodeURIComponent(this.databaseInfo.apiKey)}`;
     }
     return url;
   }
diff --git a/packages/firestore/test/unit/remote/web_channel_connection.browser.test.ts b/packages/firestore/test/unit/remote/web_channel_connection.browser.test.ts
new file mode 100644
index 00000000000..73f6ddf03d8
--- /dev/null
+++ b/packages/firestore/test/unit/remote/web_channel_connection.browser.test.ts
@@ -0,0 +1,71 @@
+/**
+ * @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 { expect } from 'chai';
+
+import { DatabaseId, DatabaseInfo } from '../../../src/core/database_info';
+import { WebChannelConnection } from '../../../src/platform/browser/webchannel_connection';
+import {
+  WebChannelOptions,
+  WebChannelTransport
+} from '@firebase/webchannel-wrapper';
+
+export class TestWebChannelConnection extends WebChannelConnection {
+  public transport: { lastOptions?: WebChannelOptions } & WebChannelTransport =
+    {
+      lastOptions: undefined,
+      createWebChannel(url: string, options: WebChannelOptions): never {
+        this.lastOptions = options;
+
+        // Throw here so we don't have to mock out any more of Web Channel
+        throw new Error('Not implemented for test');
+      }
+    };
+  protected createWebChannelTransport(): WebChannelTransport {
+    return this.transport;
+  }
+}
+
+describe('WebChannelConnection', () => {
+  const testDatabaseInfo = new DatabaseInfo(
+    new DatabaseId('testproject'),
+    'test-app-id',
+    'persistenceKey',
+    'example.com',
+    /*ssl=*/ false,
+    /*forceLongPolling=*/ false,
+    /*autoDetectLongPolling=*/ false,
+    /*longPollingOptions=*/ {},
+    /*useFetchStreams=*/ false,
+    /*isUsingEmulator=*/ false,
+    'wc-connection-test-api-key'
+  );
+
+  it('Passes the API Key from DatabaseInfo to makeHeaders for openStream', async () => {
+    const connection = new TestWebChannelConnection(testDatabaseInfo);
+
+    expect(() => connection.openStream('mockRpc', null, null)).to.throw(
+      'Not implemented for test'
+    );
+
+    const headers = connection.transport.lastOptions
+      ?.initMessageHeaders as unknown as { [key: string]: string };
+    expect(headers['x-goog-api-key']).to.deep.equal(
+      'wc-connection-test-api-key'
+    );
+  });
+});