diff --git a/src/auth/oauth2client.ts b/src/auth/oauth2client.ts
index 31af6a9c..2187461d 100644
--- a/src/auth/oauth2client.ts
+++ b/src/auth/oauth2client.ts
@@ -742,15 +742,6 @@ export class OAuth2Client extends AuthClient {
    */
   async getRequestHeaders(url?: string): Promise<Headers> {
     const headers = (await this.getRequestMetadataAsync(url)).headers;
-    // quota_project_id, stored in application_default_credentials.json, is set in
-    // the x-goog-user-project header, to indicate an alternate account for
-    // billing and quota:
-    if (
-      !headers['x-goog-user-project'] && // don't override a value the user sets.
-      this.quotaProjectId
-    ) {
-      headers['x-goog-user-project'] = this.quotaProjectId;
-    }
     return headers;
   }
 
@@ -793,9 +784,20 @@ export class OAuth2Client extends AuthClient {
     credentials.token_type = credentials.token_type || 'Bearer';
     tokens.refresh_token = credentials.refresh_token;
     this.credentials = tokens;
-    const headers = {
+    const headers: {[index: string]: string} = {
       Authorization: credentials.token_type + ' ' + tokens.access_token,
     };
+
+    // quota_project_id, stored in application_default_credentials.json, is set in
+    // the x-goog-user-project header, to indicate an alternate account for
+    // billing and quota:
+    if (
+      !headers['x-goog-user-project'] && // don't override a value the user sets.
+      this.quotaProjectId
+    ) {
+      headers['x-goog-user-project'] = this.quotaProjectId;
+    }
+
     return {headers, res: r.res};
   }
 
@@ -896,12 +898,14 @@ export class OAuth2Client extends AuthClient {
     let r2: GaxiosResponse;
     try {
       const r = await this.getRequestMetadataAsync(opts.url);
+      opts.headers = opts.headers || {};
+      if (r.headers?.['x-goog-user-project']) {
+        opts.headers['x-goog-user-project'] = r.headers['x-goog-user-project'];
+      }
       if (r.headers && r.headers.Authorization) {
-        opts.headers = opts.headers || {};
         opts.headers.Authorization = r.headers.Authorization;
       }
       if (this.apiKey) {
-        opts.headers = opts.headers || {};
         opts.headers['X-Goog-Api-Key'] = this.apiKey;
       }
       r2 = await this.transporter.request<T>(opts);
diff --git a/test/test.googleauth.ts b/test/test.googleauth.ts
index 5777c6fb..4ae37080 100644
--- a/test/test.googleauth.ts
+++ b/test/test.googleauth.ts
@@ -1444,54 +1444,70 @@ describe('googleauth', () => {
   });
 
   it('getRequestHeaders populates x-goog-user-project with quota_project if present', async () => {
-    // Fake a home directory in our fixtures path.
-    mockEnvVar('GCLOUD_PROJECT', 'my-fake-project');
-    mockEnvVar('HOME', './test/fixtures/config-with-quota');
-    mockEnvVar('APPDATA', './test/fixtures/config-with-quota/.config');
-    // The first time auth.getClient() is called /token endpoint is used to
-    // fetch a JWT.
-    const req = nock('https://oauth2.googleapis.com')
-      .post('/token')
-      .reply(200, {});
-
+    const tokenReq = mockApplicationDefaultCredentials(
+      './test/fixtures/config-with-quota'
+    );
     const auth = new GoogleAuth();
     const headers = await auth.getRequestHeaders();
     assert.strictEqual(headers['x-goog-user-project'], 'my-quota-project');
-    req.done();
+    tokenReq.done();
   });
 
   it('getRequestHeaders does not populate x-goog-user-project if quota_project is not present', async () => {
-    // Fake a home directory in our fixtures path.
-    mockEnvVar('GCLOUD_PROJECT', 'my-fake-project');
-    mockEnvVar('HOME', './test/fixtures/config-no-quota');
-    mockEnvVar('APPDATA', './test/fixtures/config-no-quota/.config');
-    // The first time auth.getClient() is called /token endpoint is used to
-    // fetch a JWT.
-    const req = nock('https://oauth2.googleapis.com')
-      .post('/token')
-      .reply(200, {});
-
+    const tokenReq = mockApplicationDefaultCredentials(
+      './test/fixtures/config-no-quota'
+    );
     const auth = new GoogleAuth();
     const headers = await auth.getRequestHeaders();
     assert.strictEqual(headers['x-goog-user-project'], undefined);
-    req.done();
+    tokenReq.done();
   });
 
   it('getRequestHeaders populates x-goog-user-project when called on returned client', async () => {
+    const tokenReq = mockApplicationDefaultCredentials(
+      './test/fixtures/config-with-quota'
+    );
+    const auth = new GoogleAuth();
+    const client = await auth.getClient();
+    const headers = await client.getRequestHeaders();
+    assert.strictEqual(headers['x-goog-user-project'], 'my-quota-project');
+    tokenReq.done();
+  });
+
+  it('populates x-goog-user-project when request is made', async () => {
+    const tokenReq = mockApplicationDefaultCredentials(
+      './test/fixtures/config-with-quota'
+    );
+    const auth = new GoogleAuth();
+    const client = await auth.getClient();
+    const apiReq = nock(BASE_URL)
+      .post(ENDPOINT)
+      .reply(function(uri) {
+        assert.strictEqual(
+          this.req.headers['x-goog-user-project'][0],
+          'my-quota-project'
+        );
+        return [200, RESPONSE_BODY];
+      });
+    const res = await client.request({
+      url: BASE_URL + ENDPOINT,
+      method: 'POST',
+      data: {test: true},
+    });
+    assert.strictEqual(RESPONSE_BODY, res.data);
+    tokenReq.done();
+    apiReq.done();
+  });
+
+  function mockApplicationDefaultCredentials(path: string) {
     // Fake a home directory in our fixtures path.
     mockEnvVar('GCLOUD_PROJECT', 'my-fake-project');
-    mockEnvVar('HOME', './test/fixtures/config-with-quota');
-    mockEnvVar('APPDATA', './test/fixtures/config-with-quota/.config');
+    mockEnvVar('HOME', path);
+    mockEnvVar('APPDATA', `${path}/.config`);
     // The first time auth.getClient() is called /token endpoint is used to
     // fetch a JWT.
-    const req = nock('https://oauth2.googleapis.com')
+    return nock('https://oauth2.googleapis.com')
       .post('/token')
       .reply(200, {});
-
-    const auth = new GoogleAuth();
-    const client = await auth.getClient();
-    const headers = await client.getRequestHeaders();
-    assert.strictEqual(headers['x-goog-user-project'], 'my-quota-project');
-    req.done();
-  });
+  }
 });