--- a/devtools/client/shared/test/browser.ini
+++ b/devtools/client/shared/test/browser.ini
@@ -33,16 +33,17 @@ support-files =
   leakhunt.js
   shared-head.js
   shared-redux-head.js
   telemetry-test-helpers.js
   test-actor-registry.js
   test-actor.js
   !/devtools/client/responsive.html/test/browser/devices.json
 
+[browser_autocomplete_popup.js]
 [browser_css_angle.js]
 [browser_css_color.js]
 [browser_cubic-bezier-01.js]
 [browser_cubic-bezier-02.js]
 [browser_cubic-bezier-03.js]
 [browser_cubic-bezier-04.js]
 [browser_cubic-bezier-05.js]
 [browser_cubic-bezier-06.js]

rename from devtools/client/webconsole/test/mochitest/browser_jsterm_popup.js
rename to devtools/client/shared/test/browser_autocomplete_popup.js
--- a/devtools/client/webconsole/test/mochitest/browser_jsterm_popup.js
+++ b/devtools/client/shared/test/browser_autocomplete_popup.js
@@ -1,25 +1,27 @@
-/* -*- indent-tabs-mode: nil; js-indent-level: 2 -*- */
-/* vim: set ft=javascript ts=2 et sw=2 tw=80: */
 /* Any copyright is dedicated to the Public Domain.
  * http://creativecommons.org/publicdomain/zero/1.0/ */
 
 "use strict";
 
-// See Bug 585991.
-
-const TEST_URI = "data:text/html;charset=utf-8,<p>bug 585991 - autocomplete popup test";
+add_task(async function() {
+  const AutocompletePopup = require("devtools/client/shared/autocomplete-popup");
 
-add_task(async function() {
-  const {jsterm} = await openNewTabAndConsole(TEST_URI);
-  const {
-    autocompletePopup: popup,
-    inputNode: input,
-  } = jsterm;
+  info("Create an autocompletion popup");
+  const [,, doc] = await createHost();
+  const input = doc.createElement("input");
+  doc.body.appendChild(input);
+
+  const autocompleteOptions = {
+    position: "top",
+    autoSelect: true
+  };
+  const popup = new AutocompletePopup(doc, autocompleteOptions);
+  input.focus();
 
   const items = [
     {label: "item0", value: "value0"},
     {label: "item1", value: "value1"},
     {label: "item2", value: "value2"},
   ];
 
   ok(!popup.isOpen, "popup is not open");

--- a/devtools/client/webconsole/test/mochitest/browser.ini
+++ b/devtools/client/webconsole/test/mochitest/browser.ini
@@ -222,17 +222,16 @@ skip-if = os != 'mac' # The tested ctrl+
 [browser_jsterm_inspect.js]
 [browser_jsterm_instance_of.js]
 [browser_jsterm_multiline.js]
 [browser_jsterm_no_autocompletion_on_defined_variables.js]
 [browser_jsterm_no_input_and_tab_key_pressed.js]
 [browser_jsterm_no_input_change_and_tab_key_pressed.js]
 [browser_jsterm_null_undefined.js]
 [browser_jsterm_popup_close_on_tab_switch.js]
-[browser_jsterm_popup.js]
 [browser_jsterm_screenshot_command_clipboard.js]
 subsuite = clipboard
 [browser_jsterm_screenshot_command_file.js]
 skip-if = (os == 'win') # Bug 1464461, disabled on Win due to timeouts
 [browser_jsterm_selfxss.js]
 subsuite = clipboard
 [browser_webconsole_allow_mixedcontent_securityerrors.js]
 tags = mcb

--- a/devtools/client/webconsole/test/mochitest/browser_jsterm_accessibility.js
+++ b/devtools/client/webconsole/test/mochitest/browser_jsterm_accessibility.js
@@ -14,18 +14,26 @@ add_task(async function() {
   const hud = await openNewTabAndConsole(TEST_URI);
 
   const jsterm = hud.jsterm;
   const input = jsterm.inputNode;
 
   info("Test that the console input is not treated as a live region");
   ok(!isElementInLiveRegion(input), "Console input is not treated as a live region");
 
+  info("Test the console input has no aria-activedescendant attribute");
+  ok(!input.hasAttribute("aria-activedescendant"), "no aria-activedescendant");
+
   info("Type 'd' to open the autocomplete popup");
-  await autocomplete(jsterm, "d");
+  const onPopupOpen = jsterm.autocompletePopup.once("popup-opened");
+  autocomplete(jsterm, "d");
+  await onPopupOpen;
+
+  info("Test the console input has an aria-activedescendant attribute");
+  ok(input.hasAttribute("aria-activedescendant"), "aria-activedescendant");
 
   // Add listeners for focus and blur events.
   let wasBlurred = false;
   input.addEventListener("blur", () => {
     wasBlurred = true;
   }, {
     once: true
   });
@@ -41,16 +49,19 @@ add_task(async function() {
   info("Close the autocomplete popup by simulating a TAB key event");
   const onPopupClosed = jsterm.autocompletePopup.once("popup-closed");
   EventUtils.synthesizeKey("KEY_Tab");
 
   info("Wait for the autocomplete popup to be closed");
   await onPopupClosed;
 
   ok(wasFocused, "jsterm input received a focus event");
+
+  info("Test the console input has no aria-activedescendant attribute no more");
+  ok(!input.hasAttribute("aria-activedescendant"), "no aria-activedescendant");
 });
 
 async function autocomplete(jsterm, value) {
   const popup = jsterm.autocompletePopup;
 
   await new Promise(resolve => {
     jsterm.setInputValue(value);
     jsterm.complete(jsterm.COMPLETE_HINT_ONLY, resolve);