diff --git a/browser/components/urlbar/moz.build b/browser/components/urlbar/moz.build
index 3d61f4217d2e..3b8343cd6af1 100644
--- a/browser/components/urlbar/moz.build
+++ b/browser/components/urlbar/moz.build
@@ -14,4 +14,5 @@ EXTRA_JS_MODULES += [
     'UrlbarView.jsm',
 ]
 
+BROWSER_CHROME_MANIFESTS += ['tests/browser/browser.ini']
 XPCSHELL_TESTS_MANIFESTS += ['tests/unit/xpcshell.ini']
diff --git a/browser/components/urlbar/tests/browser/.eslintrc.js b/browser/components/urlbar/tests/browser/.eslintrc.js
new file mode 100644
index 000000000000..b1c842d8a6db
--- /dev/null
+++ b/browser/components/urlbar/tests/browser/.eslintrc.js
@@ -0,0 +1,7 @@
+"use strict";
+
+module.exports = {
+  "extends": [
+    "plugin:mozilla/browser-test"
+  ]
+};
diff --git a/browser/components/urlbar/tests/browser/browser.ini b/browser/components/urlbar/tests/browser/browser.ini
new file mode 100644
index 000000000000..75dc42e7acbd
--- /dev/null
+++ b/browser/components/urlbar/tests/browser/browser.ini
@@ -0,0 +1,8 @@
+# This Source Code Form is subject to the terms of the Mozilla Public
+# License, v. 2.0. If a copy of the MPL was not distributed with this
+# file, You can obtain one at http://mozilla.org/MPL/2.0/.
+
+[DEFAULT]
+
+[browser_UrlbarInput_unit.js]
+support-files = empty.xul
diff --git a/browser/components/urlbar/tests/unit/test_UrlbarInput_unit.js b/browser/components/urlbar/tests/browser/browser_UrlbarInput_unit.js
similarity index 73%
rename from browser/components/urlbar/tests/unit/test_UrlbarInput_unit.js
rename to browser/components/urlbar/tests/browser/browser_UrlbarInput_unit.js
index 408e6c25cf14..3b594a6a983f 100644
--- a/browser/components/urlbar/tests/unit/test_UrlbarInput_unit.js
+++ b/browser/components/urlbar/tests/browser/browser_UrlbarInput_unit.js
@@ -14,7 +14,14 @@ let generalListener;
 let input;
 let inputOptions;
 
-ChromeUtils.import("resource://gre/modules/PrivateBrowsingUtils.jsm");
+ChromeUtils.import("resource:///modules/UrlbarController.jsm", this);
+
+/* global sinon */
+Services.scriptloader.loadSubScript("resource://testing-common/sinon-2.3.2.js");
+
+registerCleanupFunction(function() {
+  delete window.sinon;
+});
 
 /**
  * Asserts that the query context has the expected values.
@@ -32,15 +39,6 @@ function assertContextMatches(context, expectedValues) {
   }
 }
 
-/**
- * @returns {object} A fake element with minimal functions for simulating textbox etc.
- */
-function createFakeElement() {
-  return {
-    addEventListener() {},
-  };
-}
-
 /**
  * Checks the result of a handleQuery call on the controller.
  *
@@ -68,7 +66,7 @@ function checkHandleQueryCall(stub, expectedQueryContextProps) {
   }
 }
 
-add_task(function setup() {
+add_task(async function setup() {
   sandbox = sinon.sandbox.create();
 
   fakeController = new UrlbarController();
@@ -76,17 +74,30 @@ add_task(function setup() {
   sandbox.stub(fakeController, "handleQuery");
   sandbox.stub(PrivateBrowsingUtils, "isWindowPrivate").returns(false);
 
-  let textbox = createFakeElement();
-  textbox.inputField = createFakeElement();
-  textbox.inputField.controllers = { insertControllerAt() {} };
+  // Open a new window, so we don't affect other tests by adding extra
+  // UrbarInput wrappers around the urlbar.
+  let gTestRoot = getRootDirectory(gTestPath);
+
+  let win = window.openDialog(gTestRoot + "empty.xul",
+                    "", "chrome");
+  await BrowserTestUtils.waitForEvent(win, "load");
+
+  registerCleanupFunction(async () => {
+    await BrowserTestUtils.closeWindow(win);
+    sandbox.restore();
+  });
+
+  // Clone the elements into the new window, so we get exact copies without having
+  // to replicate the xul.
+  let doc = win.document;
+  let textbox = doc.importNode(document.getElementById("urlbar"), true);
+  doc.documentElement.appendChild(textbox);
+  let panel = doc.importNode(document.getElementById("urlbar-results"), true);
+  doc.documentElement.appendChild(panel);
+
   inputOptions = {
     textbox,
-    panel: {
-      ownerDocument: {},
-      querySelector() {
-        return createFakeElement();
-      },
-    },
+    panel,
     controller: fakeController,
   };
 
diff --git a/browser/components/urlbar/tests/browser/empty.xul b/browser/components/urlbar/tests/browser/empty.xul
new file mode 100644
index 000000000000..fd9d8e5c78b8
--- /dev/null
+++ b/browser/components/urlbar/tests/browser/empty.xul
@@ -0,0 +1,2 @@
+<?xml version="1.0"?>
+<window xmlns="http://www.mozilla.org/keymaster/gatekeeper/there.is.only.xul"/>
diff --git a/browser/components/urlbar/tests/unit/xpcshell.ini b/browser/components/urlbar/tests/unit/xpcshell.ini
index 3f8f41362ec8..3aeabecb67c7 100644
--- a/browser/components/urlbar/tests/unit/xpcshell.ini
+++ b/browser/components/urlbar/tests/unit/xpcshell.ini
@@ -6,4 +6,3 @@ firefox-appdir = browser
 [test_tokenizer.js]
 [test_UrlbarController_unit.js]
 [test_UrlbarController_integration.js]
-[test_UrlbarInput_unit.js]