diff --git a/src/components/views/elements/AppTile.tsx b/src/components/views/elements/AppTile.tsx
index 6f7267b3d8c..05c67ab9413 100644
--- a/src/components/views/elements/AppTile.tsx
+++ b/src/components/views/elements/AppTile.tsx
@@ -35,7 +35,7 @@ import SettingsStore from "../../../settings/SettingsStore";
 import { aboveLeftOf, ContextMenuButton } from "../../structures/ContextMenu";
 import PersistedElement, { getPersistKey } from "./PersistedElement";
 import { WidgetType } from "../../../widgets/WidgetType";
-import { StopGapWidget } from "../../../stores/widgets/StopGapWidget";
+import { ElementWidget, StopGapWidget } from "../../../stores/widgets/StopGapWidget";
 import { ElementWidgetActions } from "../../../stores/widgets/ElementWidgetActions";
 import WidgetContextMenu from "../context_menus/WidgetContextMenu";
 import WidgetAvatar from "../avatars/WidgetAvatar";
@@ -50,6 +50,7 @@ import MatrixClientContext from "../../../contexts/MatrixClientContext";
 import { ActionPayload } from "../../../dispatcher/payloads";
 import { Action } from '../../../dispatcher/actions';
 import { ElementWidgetCapabilities } from '../../../stores/widgets/ElementWidgetCapabilities';
+import { WidgetMessagingStore } from '../../../stores/widgets/WidgetMessagingStore';
 
 interface IProps {
     app: IApp;
@@ -196,6 +197,24 @@ export default class AppTile extends React.Component<IProps, IState> {
         }
     };
 
+    private determineInitialRequiresClientState(): boolean {
+        try {
+            const mockWidget = new ElementWidget(this.props.app);
+            const widgetApi = WidgetMessagingStore.instance.getMessaging(mockWidget, this.props.room.roomId);
+            if (widgetApi) {
+                // Load value from existing API to prevent resetting the requiresClient value on layout changes.
+                return widgetApi.hasCapability(ElementWidgetCapabilities.RequiresClient);
+            }
+        } catch {
+            // fallback to true
+        }
+
+        // requiresClient is initially set to true. This avoids the broken state of the popout
+        // button being visible (for an instance) and then disappearing when the widget is loaded.
+        // requiresClient <-> hide the popout button
+        return true;
+    }
+
     /**
      * Set initial component state when the App wUrl (widget URL) is being updated.
      * Component props *must* be passed (rather than relying on this.props).
@@ -214,10 +233,7 @@ export default class AppTile extends React.Component<IProps, IState> {
             error: null,
             menuDisplayed: false,
             widgetPageTitle: this.props.widgetPageTitle,
-            // requiresClient is initially set to true. This avoids the broken state of the popout
-            // button being visible (for an instance) and then disappearing when the widget is loaded.
-            // requiresClient <-> hide the popout button
-            requiresClient: true,
+            requiresClient: this.determineInitialRequiresClientState(),
         };
     }
 
diff --git a/test/components/views/elements/AppTile-test.tsx b/test/components/views/elements/AppTile-test.tsx
index 207623833fe..d528f52a9ee 100644
--- a/test/components/views/elements/AppTile-test.tsx
+++ b/test/components/views/elements/AppTile-test.tsx
@@ -18,7 +18,7 @@ import React from "react";
 import TestRenderer from "react-test-renderer";
 import { jest } from "@jest/globals";
 import { Room } from "matrix-js-sdk/src/models/room";
-import { MatrixWidgetType } from "matrix-widget-api";
+import { ClientWidgetApi, MatrixWidgetType } from "matrix-widget-api";
 import { mount, ReactWrapper } from "enzyme";
 import { Optional } from "matrix-events-sdk";
 
@@ -39,11 +39,14 @@ import ActiveWidgetStore from "../../../../src/stores/ActiveWidgetStore";
 import AppTile from "../../../../src/components/views/elements/AppTile";
 import { Container, WidgetLayoutStore } from "../../../../src/stores/widgets/WidgetLayoutStore";
 import AppsDrawer from "../../../../src/components/views/rooms/AppsDrawer";
+import { ElementWidgetCapabilities } from "../../../../src/stores/widgets/ElementWidgetCapabilities";
+import { ElementWidget } from "../../../../src/stores/widgets/StopGapWidget";
+import { WidgetMessagingStore } from "../../../../src/stores/widgets/WidgetMessagingStore";
 
 describe("AppTile", () => {
     let cli;
-    let r1;
-    let r2;
+    let r1: Room;
+    let r2: Room;
     const resizeNotifier = new ResizeNotifier();
     let app1: IApp;
     let app2: IApp;
@@ -328,6 +331,10 @@ describe("AppTile", () => {
             moveToContainerSpy = jest.spyOn(WidgetLayoutStore.instance, 'moveToContainer');
         });
 
+        it("requiresClient should be true", () => {
+            expect(wrapper.state('requiresClient')).toBe(true);
+        });
+
         it("clicking 'minimise' should send the widget to the right", () => {
             const minimiseButton = wrapper.find('.mx_AppTileMenuBar_iconButton_minimise');
             minimiseButton.first().simulate('click');
@@ -355,5 +362,35 @@ describe("AppTile", () => {
                 expect(moveToContainerSpy).toHaveBeenCalledWith(r1, app1, Container.Top);
             });
         });
+
+        describe("with an existing widgetApi holding requiresClient = false", () => {
+            let wrapper: ReactWrapper;
+
+            beforeEach(() => {
+                const api = {
+                    hasCapability: (capability: ElementWidgetCapabilities): boolean => {
+                        return !(capability === ElementWidgetCapabilities.RequiresClient);
+                    },
+                    once: () => {},
+                } as unknown as ClientWidgetApi;
+
+                const mockWidget = new ElementWidget(app1);
+                WidgetMessagingStore.instance.storeMessaging(mockWidget, r1.roomId, api);
+
+                wrapper = mount((
+                    <MatrixClientContext.Provider value={cli}>
+                        <AppTile
+                            key={app1.id}
+                            app={app1}
+                            room={r1}
+                        />
+                    </MatrixClientContext.Provider>
+                ));
+            });
+
+            it("requiresClient should be false", () => {
+                expect(wrapper.state('requiresClient')).toBe(false);
+            });
+        });
     });
 });