diff --git a/src/components/views/context_menus/WidgetContextMenu.tsx b/src/components/views/context_menus/WidgetContextMenu.tsx
index 8026942038..3c7bf0ee0e 100644
--- a/src/components/views/context_menus/WidgetContextMenu.tsx
+++ b/src/components/views/context_menus/WidgetContextMenu.tsx
@@ -127,7 +127,8 @@ const WidgetContextMenu: React.FC<IProps> = ({
             console.info("Revoking permission for widget to load: " + app.eventId);
             const current = SettingsStore.getValue("allowedWidgets", roomId);
             current[app.eventId] = false;
-            SettingsStore.setValue("allowedWidgets", roomId, SettingLevel.ROOM_ACCOUNT, current).catch(err => {
+            const level = SettingsStore.firstSupportedLevel("allowedWidgets");
+            SettingsStore.setValue("allowedWidgets", roomId, level, current).catch(err => {
                 console.error(err);
                 // We don't really need to do anything about this - the user will just hit the button again.
             });
diff --git a/src/components/views/elements/AppTile.js b/src/components/views/elements/AppTile.js
index 7e0ae965bb..65bc0ac6f1 100644
--- a/src/components/views/elements/AppTile.js
+++ b/src/components/views/elements/AppTile.js
@@ -240,7 +240,8 @@ export default class AppTile extends React.Component {
         console.info("Granting permission for widget to load: " + this.props.app.eventId);
         const current = SettingsStore.getValue("allowedWidgets", roomId);
         current[this.props.app.eventId] = true;
-        SettingsStore.setValue("allowedWidgets", roomId, SettingLevel.ROOM_ACCOUNT, current).then(() => {
+        const level = SettingsStore.firstSupportedLevel("allowedWidgets");
+        SettingsStore.setValue("allowedWidgets", roomId, level, current).then(() => {
             this.setState({hasPermissionToLoad: true});
 
             // Fetch a token for the integration manager, now that we're allowed to
diff --git a/src/settings/Settings.ts b/src/settings/Settings.ts
index b239b809fe..6ca009df61 100644
--- a/src/settings/Settings.ts
+++ b/src/settings/Settings.ts
@@ -421,7 +421,8 @@ export const SETTINGS: {[setting: string]: ISetting} = {
         default: true,
     },
     "allowedWidgets": {
-        supportedLevels: [SettingLevel.ROOM_ACCOUNT],
+        supportedLevels: [SettingLevel.ROOM_ACCOUNT, SettingLevel.ROOM_DEVICE],
+        supportedLevelsAreOrdered: true,
         default: {}, // none allowed
     },
     "analyticsOptIn": {
diff --git a/src/settings/SettingsStore.ts b/src/settings/SettingsStore.ts
index 82f169f498..2d024ba3f8 100644
--- a/src/settings/SettingsStore.ts
+++ b/src/settings/SettingsStore.ts
@@ -467,6 +467,31 @@ export default class SettingsStore {
         return LEVEL_HANDLERS[level].isSupported();
     }
 
+    /**
+     * Determines the first supported level out of all the levels that can be used for a
+     * specific setting.
+     * @param {string} settingName The setting name.
+     * @return {SettingLevel}
+     */
+    public static firstSupportedLevel(settingName: string): SettingLevel {
+        // Verify that the setting is actually a setting
+        const setting = SETTINGS[settingName];
+        if (!setting) {
+            throw new Error("Setting '" + settingName + "' does not appear to be a setting.");
+        }
+
+        const levelOrder = (setting.supportedLevelsAreOrdered ? setting.supportedLevels : LEVEL_ORDER);
+        if (!levelOrder.includes(SettingLevel.DEFAULT)) levelOrder.push(SettingLevel.DEFAULT); // always include default
+
+        const handlers = SettingsStore.getHandlers(settingName);
+
+        for (const level of levelOrder) {
+            const handler = handlers[level];
+            if (!handler) continue;
+            return level;
+        }
+    }
+
     /**
      * Debugging function for reading explicit setting values without going through the
      * complicated/biased functions in the SettingsStore. This will print information to