diff --git a/src/components/views/elements/AppTile.tsx b/src/components/views/elements/AppTile.tsx
index 5f7c0543c4..d8a29e81fc 100644
--- a/src/components/views/elements/AppTile.tsx
+++ b/src/components/views/elements/AppTile.tsx
@@ -84,6 +84,7 @@ interface IState {
     error: Error;
     menuDisplayed: boolean;
     widgetPageTitle: string;
+    requiresClient: boolean;
 }
 
 import { logger } from "matrix-js-sdk/src/logger";
@@ -114,8 +115,10 @@ export default class AppTile extends React.Component<IProps, IState> {
         this.persistKey = getPersistKey(this.props.app.id);
         try {
             this.sgWidget = new StopGapWidget(this.props);
-            this.sgWidget.on("preparing", this.onWidgetPrepared);
+            this.sgWidget.on("preparing", this.onWidgetPreparing);
             this.sgWidget.on("ready", this.onWidgetReady);
+            // emits when the capabilites have been setup or changed
+            this.sgWidget.on("capabilitiesNotified", this.onWidgetCapabilitiesNotified);
         } catch (e) {
             logger.log("Failed to construct widget", e);
             this.sgWidget = null;
@@ -155,6 +158,10 @@ 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,
         };
     }
 
@@ -216,7 +223,7 @@ export default class AppTile extends React.Component<IProps, IState> {
         }
         try {
             this.sgWidget = new StopGapWidget(newProps);
-            this.sgWidget.on("preparing", this.onWidgetPrepared);
+            this.sgWidget.on("preparing", this.onWidgetPreparing);
             this.sgWidget.on("ready", this.onWidgetReady);
             this.startWidget();
         } catch (e) {
@@ -287,7 +294,7 @@ export default class AppTile extends React.Component<IProps, IState> {
         if (this.sgWidget) this.sgWidget.stop({ forceDestroy: true });
     }
 
-    private onWidgetPrepared = (): void => {
+    private onWidgetPreparing = (): void => {
         this.setState({ loading: false });
     };
 
@@ -297,6 +304,12 @@ export default class AppTile extends React.Component<IProps, IState> {
         }
     };
 
+    private onWidgetCapabilitiesNotified = (): void => {
+        this.setState({
+            requiresClient: this.sgWidget.widgetApi.hasCapability(MatrixCapabilities.RequiresClient),
+        });
+    };
+
     private onAction = (payload): void => {
         if (payload.widgetId === this.props.app.id) {
             switch (payload.action) {
@@ -512,7 +525,7 @@ export default class AppTile extends React.Component<IProps, IState> {
                             { this.props.showTitle && this.getTileTitle() }
                         </span>
                         <span className="mx_AppTileMenuBarWidgets">
-                            { this.props.showPopout && <AccessibleButton
+                            { (this.props.showPopout && !this.state.requiresClient) && <AccessibleButton
                                 className="mx_AppTileMenuBar_iconButton mx_AppTileMenuBar_iconButton_popout"
                                 title={_t('Popout widget')}
                                 onClick={this.onPopoutWidgetClick}
diff --git a/src/stores/widgets/StopGapWidget.ts b/src/stores/widgets/StopGapWidget.ts
index 1293fe0548..b08b51a32f 100644
--- a/src/stores/widgets/StopGapWidget.ts
+++ b/src/stores/widgets/StopGapWidget.ts
@@ -135,7 +135,7 @@ export class ElementWidget extends Widget {
         };
     }
 
-    public getCompleteUrl(params: ITemplateParams, asPopout=false): string {
+    public getCompleteUrl(params: ITemplateParams, asPopout = false): string {
         return runTemplate(asPopout ? this.popoutTemplateUrl : this.templateUrl, {
             ...this.rawDefinition,
             data: this.rawData,
@@ -149,7 +149,7 @@ export class StopGapWidget extends EventEmitter {
     private scalarToken: string;
     private roomId?: string;
     private kind: WidgetKind;
-    private readUpToMap: {[roomId: string]: string} = {}; // room ID to event ID
+    private readUpToMap: { [roomId: string]: string } = {}; // room ID to event ID
 
     constructor(private appTileProps: IAppTileProps) {
         super();
@@ -262,6 +262,7 @@ export class StopGapWidget extends EventEmitter {
         this.messaging = new ClientWidgetApi(this.mockWidget, iframe, driver);
         this.messaging.on("preparing", () => this.emit("preparing"));
         this.messaging.on("ready", () => this.emit("ready"));
+        this.messaging.on("capabilitiesNotified", () => this.emit("capabilitiesNotified"));
         this.messaging.on(`action:${WidgetApiFromWidgetAction.OpenModalWidget}`, this.onOpenModal);
         WidgetMessagingStore.instance.storeMessaging(this.mockWidget, this.messaging);
 
diff --git a/src/stores/widgets/StopGapWidgetDriver.ts b/src/stores/widgets/StopGapWidgetDriver.ts
index e8f550b92c..da844b1923 100644
--- a/src/stores/widgets/StopGapWidgetDriver.ts
+++ b/src/stores/widgets/StopGapWidgetDriver.ts
@@ -73,7 +73,9 @@ export class StopGapWidgetDriver extends WidgetDriver {
         // Always allow screenshots to be taken because it's a client-induced flow. The widget can't
         // spew screenshots at us and can't request screenshots of us, so it's up to us to provide the
         // button if the widget says it supports screenshots.
-        this.allowedCapabilities = new Set([...allowedCapabilities, MatrixCapabilities.Screenshots]);
+        this.allowedCapabilities = new Set([...allowedCapabilities,
+            MatrixCapabilities.Screenshots,
+            MatrixCapabilities.RequiresClient]);
 
         // Grant the permissions that are specific to given widget types
         if (WidgetType.JITSI.matches(this.forWidget.type) && forWidgetKind === WidgetKind.Room) {