diff --git a/browser/components/extensions/test/browser/browser-common.ini b/browser/components/extensions/test/browser/browser-common.ini
index 3d22c692412d..e99d40e1e494 100644
--- a/browser/components/extensions/test/browser/browser-common.ini
+++ b/browser/components/extensions/test/browser/browser-common.ini
@@ -56,7 +56,6 @@ skip-if = (os == 'win' && !debug) # bug 1352668
 [browser_ext_contextMenus_checkboxes.js]
 [browser_ext_contextMenus_commands.js]
 [browser_ext_contextMenus_icons.js]
-skip-if = os == 'win' && !debug # Bug 1351638
 [browser_ext_contextMenus_onclick.js]
 [browser_ext_contextMenus_radioGroups.js]
 [browser_ext_contextMenus_uninstall.js]
diff --git a/browser/components/extensions/test/browser/browser_ext_contextMenus_commands.js b/browser/components/extensions/test/browser/browser_ext_contextMenus_commands.js
index 39587c11fb84..355be93c43bf 100644
--- a/browser/components/extensions/test/browser/browser_ext_contextMenus_commands.js
+++ b/browser/components/extensions/test/browser/browser_ext_contextMenus_commands.js
@@ -33,6 +33,7 @@ add_task(async function() {
 
   let extension = ExtensionTestUtils.loadExtension({
     manifest: {
+      "name": "contextMenus commands",
       "permissions": ["contextMenus", "activeTab", "tabs"],
       "browser_action": {
         "default_title": "Test BrowserAction",
@@ -59,6 +60,7 @@ add_task(async function() {
   async function testContext(id) {
     const menu = await openExtensionContextMenu();
     const items = menu.getElementsByAttribute("label", id);
+    is(items.length, 1, `exactly one menu item found`);
     await closeExtensionContextMenu(items[0]);
     return extension.awaitMessage("test-opened");
   }
diff --git a/browser/components/extensions/test/browser/browser_ext_contextMenus_icons.js b/browser/components/extensions/test/browser/browser_ext_contextMenus_icons.js
index 0f963160a5ab..a659336f8d94 100644
--- a/browser/components/extensions/test/browser/browser_ext_contextMenus_icons.js
+++ b/browser/components/extensions/test/browser/browser_ext_contextMenus_icons.js
@@ -11,6 +11,7 @@ add_task(async function() {
 
   let extension = ExtensionTestUtils.loadExtension({
     manifest: {
+      "name": "contextMenus icons",
       "permissions": ["contextMenus"],
       "icons": {
         "18": "extension.png",
@@ -38,9 +39,10 @@ add_task(async function() {
     },
   });
 
-  let confirmContextMenuIcon = (rootElement) => {
+  let confirmContextMenuIcon = (rootElements) => {
     let expectedURL = new RegExp(String.raw`^moz-extension://[^/]+/extension\.png$`);
-    let imageUrl = rootElement.getAttribute("image");
+    is(rootElements.length, 1, "Found exactly one menu item");
+    let imageUrl = rootElements[0].getAttribute("image");
     ok(expectedURL.test(imageUrl), "The context menu should display the extension icon next to the root element");
   };
 
@@ -50,17 +52,18 @@ add_task(async function() {
   let extensionMenu = await openExtensionContextMenu();
 
   let contextMenu = document.getElementById("contentAreaContextMenu");
-  let topLevelMenuItem = contextMenu.getElementsByAttribute("ext-type", "top-level-menu")[0];
+  let topLevelMenuItem = contextMenu.getElementsByAttribute("ext-type", "top-level-menu");
   confirmContextMenuIcon(topLevelMenuItem);
 
-  let childToDelete = extensionMenu.getElementsByAttribute("label", "child-to-delete")[0];
-  await closeExtensionContextMenu(childToDelete);
+  let childToDelete = extensionMenu.getElementsByAttribute("label", "child-to-delete");
+  is(childToDelete.length, 1, "Found exactly one child to delete");
+  await closeExtensionContextMenu(childToDelete[0]);
   await extension.awaitMessage("child-deleted");
 
   await openExtensionContextMenu();
 
   contextMenu = document.getElementById("contentAreaContextMenu");
-  topLevelMenuItem = contextMenu.getElementsByAttribute("label", "child")[0];
+  topLevelMenuItem = contextMenu.getElementsByAttribute("label", "child");
 
   confirmContextMenuIcon(topLevelMenuItem);
   await closeContextMenu();
diff --git a/browser/components/extensions/test/browser/browser_ext_contextMenus_onclick.js b/browser/components/extensions/test/browser/browser_ext_contextMenus_onclick.js
index 0ca896f5c8aa..6c432de83e07 100644
--- a/browser/components/extensions/test/browser/browser_ext_contextMenus_onclick.js
+++ b/browser/components/extensions/test/browser/browser_ext_contextMenus_onclick.js
@@ -218,6 +218,7 @@ add_task(async function test_onclick_modifiers() {
   async function click(modifiers = {}) {
     const menu = await openContextMenu();
     const items = menu.getElementsByAttribute("label", "modify");
+    is(items.length, 1, "Got exactly one context menu item");
     await closeExtensionContextMenu(items[0], modifiers);
     return extension.awaitMessage("click");
   }
diff --git a/browser/components/extensions/test/browser/head.js b/browser/components/extensions/test/browser/head.js
index 8f835b63e39d..36b1889d4b5f 100644
--- a/browser/components/extensions/test/browser/head.js
+++ b/browser/components/extensions/test/browser/head.js
@@ -320,7 +320,7 @@ async function openExtensionContextMenu(selector = "#img1") {
     return null;
   }
 
-  let extensionMenu = topLevelMenu[0].childNodes[0];
+  let extensionMenu = topLevelMenu[0];
   let popupShownPromise = BrowserTestUtils.waitForEvent(contextMenu, "popupshown");
   EventUtils.synthesizeMouseAtCenter(extensionMenu, {});
   await popupShownPromise;
@@ -331,7 +331,10 @@ async function closeExtensionContextMenu(itemToSelect, modifiers = {}) {
   let contentAreaContextMenu = document.getElementById("contentAreaContextMenu");
   let popupHiddenPromise = BrowserTestUtils.waitForEvent(contentAreaContextMenu, "popuphidden");
   EventUtils.synthesizeMouseAtCenter(itemToSelect, modifiers);
-  return popupHiddenPromise;
+  await popupHiddenPromise;
+
+  // Bug 1351638: parent menu fails to close intermittently, make sure it does.
+  contentAreaContextMenu.hidePopup();
 }
 
 async function openChromeContextMenu(menuId, target, win = window) {