diff --git a/ui/app/services/token.js b/ui/app/services/token.js
index c8e5d52fab70..c11453e23401 100644
--- a/ui/app/services/token.js
+++ b/ui/app/services/token.js
@@ -1,6 +1,6 @@
 import Service, { inject as service } from '@ember/service';
 import { computed } from '@ember/object';
-import { alias } from '@ember/object/computed';
+import { alias, reads } from '@ember/object/computed';
 import { getOwner } from '@ember/application';
 import { assign } from '@ember/polyfills';
 import { task } from 'ember-concurrency';
@@ -42,6 +42,8 @@ export default class TokenService extends Service {
   })
   fetchSelfToken;
 
+  @reads('fetchSelfToken.lastSuccessful.value') selfToken;
+
   async exchangeOneTimeToken(oneTimeToken) {
     const TokenAdapter = getOwner(this).lookup('adapter:token');
 
@@ -49,12 +51,6 @@ export default class TokenService extends Service {
     this.secret = token.secret;
   }
 
-  @computed('secret', 'fetchSelfToken.lastSuccessful.value')
-  get selfToken() {
-    if (this.secret) return this.get('fetchSelfToken.lastSuccessful.value');
-    return undefined;
-  }
-
   @task(function*() {
     try {
       if (this.selfToken) {
diff --git a/ui/tests/acceptance/proxy-test.js b/ui/tests/acceptance/proxy-test.js
new file mode 100644
index 000000000000..582a57e767f1
--- /dev/null
+++ b/ui/tests/acceptance/proxy-test.js
@@ -0,0 +1,51 @@
+/* eslint-disable ember-a11y-testing/a11y-audit-called */ // Tests for non-UI behaviour.
+import { module, test } from 'qunit';
+import { setupApplicationTest } from 'ember-qunit';
+import { setupMirage } from 'ember-cli-mirage/test-support';
+import Jobs from 'nomad-ui/tests/pages/jobs/list';
+
+let managementToken;
+
+module('Acceptance | reverse proxy', function(hooks) {
+  setupApplicationTest(hooks);
+  setupMirage(hooks);
+
+  hooks.beforeEach(function() {
+    window.localStorage.clear();
+    window.sessionStorage.clear();
+
+    server.create('agent');
+    managementToken = server.create('token');
+
+    // Simulate a reverse proxy injecting X-Nomad-Token header for all requests
+    this._originalXMLHttpRequestSend = XMLHttpRequest.prototype.send;
+    (function(send) {
+      XMLHttpRequest.prototype.send = function(data) {
+        this.setRequestHeader('X-Nomad-Token', managementToken.secretId);
+        send.call(this, data);
+      };
+    })(this._originalXMLHttpRequestSend);
+  });
+
+  hooks.afterEach(function() {
+    XMLHttpRequest.prototype.send = this._originalXMLHttpRequestSend;
+  });
+
+  test('when token is inserted by a reverse proxy, the UI is adjusted', async function(assert) {
+    // when token is inserted by reserve proxy, the token is reverse proxy
+    const { secretId } = managementToken;
+
+    await Jobs.visit();
+    assert.ok(window.localStorage.nomadTokenSecret == null, 'No token secret set');
+
+    // Make sure that server received the header
+    assert.ok(
+      server.pretender.handledRequests
+        .mapBy('requestHeaders')
+        .every(headers => headers['X-Nomad-Token'] === secretId),
+      'The token header is always present'
+    );
+
+    assert.notOk(Jobs.runJobButton.isDisabled, 'Run job button is enabled');
+  });
+});