diff --git a/browser/components/extensions/child/ext-menus.js b/browser/components/extensions/child/ext-menus.js
index d9c344dfcc26c..462204a878b38 100644
--- a/browser/components/extensions/child/ext-menus.js
+++ b/browser/components/extensions/child/ext-menus.js
@@ -136,6 +136,11 @@ this.menusInternal = class extends ExtensionAPI {
             createProperties.id = ++gNextMenuItemID;
           }
           let { onclick } = createProperties;
+          if (onclick && !context.extension.persistentBackground) {
+            throw new ExtensionError(
+              `Property "onclick" cannot be used in menus.create, replace with an "onClicked" event listener.`
+            );
+          }
           delete createProperties.onclick;
           context.childManager
             .callParentAsyncFunction("menusInternal.create", [createProperties])
@@ -159,6 +164,11 @@ this.menusInternal = class extends ExtensionAPI {
 
         update(id, updateProperties) {
           let { onclick } = updateProperties;
+          if (onclick && !context.extension.persistentBackground) {
+            throw new ExtensionError(
+              `Property "onclick" cannot be used in menus.update, replace with an "onClicked" event listener.`
+            );
+          }
           delete updateProperties.onclick;
           return context.childManager
             .callParentAsyncFunction("menusInternal.update", [
diff --git a/browser/components/extensions/schemas/menus.json b/browser/components/extensions/schemas/menus.json
index b1aab5212005f..79b1511617f5d 100644
--- a/browser/components/extensions/schemas/menus.json
+++ b/browser/components/extensions/schemas/menus.json
@@ -243,6 +243,7 @@
               },
               "onclick": {
                 "type": "function",
+                "max_manifest_version": 2,
                 "optional": true,
                 "description": "A function that will be called back when the menu item is clicked. Event pages cannot use this; instead, they should register a listener for $(ref:contextMenus.onClicked).",
                 "parameters": [
@@ -374,6 +375,7 @@
               },
               "onclick": {
                 "type": "function",
+                "max_manifest_version": 2,
                 "optional": "omit-key-if-missing",
                 "parameters": [
                   {