diff --git a/src/components/views/elements/AppTile.js b/src/components/views/elements/AppTile.js
index fda2652d12..c732d8ec95 100644
--- a/src/components/views/elements/AppTile.js
+++ b/src/components/views/elements/AppTile.js
@@ -240,10 +240,14 @@ export default class AppTile extends React.Component {
             this.iframe.src = 'about:blank';
         }
 
+        if (WidgetType.JITSI.matches(this.props.app.type)) {
+            dis.dispatch({action: 'hangup_conference'});
+        }
+
         // Delete the widget from the persisted store for good measure.
         PersistedElement.destroyElement(this._persistKey);
 
-        this._sgWidget.stop();
+        this._sgWidget.stop({forceDestroy: true});
     }
 
     /* If user has permission to modify widgets, delete the widget,
@@ -387,6 +391,9 @@ export default class AppTile extends React.Component {
             if (this.props.show) {
                 // if we were being shown, end the widget as we're about to be minimized.
                 this._endWidgetActions();
+            } else {
+                // restart the widget actions
+                this._resetWidget(this.props);
             }
             dis.dispatch({
                 action: 'appsDrawer',
diff --git a/src/components/views/elements/PersistentApp.js b/src/components/views/elements/PersistentApp.js
index a3e413151a..8b2aa5c87c 100644
--- a/src/components/views/elements/PersistentApp.js
+++ b/src/components/views/elements/PersistentApp.js
@@ -58,6 +58,11 @@ export default class PersistentApp extends React.Component {
             const persistentWidgetInRoomId = ActiveWidgetStore.getRoomId(this.state.persistentWidgetId);
             if (this.state.roomId !== persistentWidgetInRoomId) {
                 const persistentWidgetInRoom = MatrixClientPeg.get().getRoom(persistentWidgetInRoomId);
+
+                // Sanity check the room - the widget may have been destroyed between render cycles, and
+                // thus no room is associated anymore.
+                if (!persistentWidgetInRoom) return null;
+
                 // get the widget data
                 const appEvent = WidgetUtils.getRoomWidgets(persistentWidgetInRoom).find((ev) => {
                     return ev.getStateKey() === ActiveWidgetStore.getPersistentWidgetId();
diff --git a/src/stores/widgets/StopGapWidget.ts b/src/stores/widgets/StopGapWidget.ts
index 1eb4f9cd27..41b040b8c6 100644
--- a/src/stores/widgets/StopGapWidget.ts
+++ b/src/stores/widgets/StopGapWidget.ts
@@ -74,6 +74,16 @@ class ElementWidget extends Widget {
         return super.templateUrl;
     }
 
+    public get popoutTemplateUrl(): string {
+        if (WidgetType.JITSI.matches(this.type)) {
+            return WidgetUtils.getLocalJitsiWrapperUrl({
+                forLocalRender: false, // The only important difference between this and templateUrl()
+                auth: super.rawData?.auth,
+            });
+        }
+        return this.templateUrl; // use this instead of super to ensure we get appropriate templating
+    }
+
     public get rawData(): IWidgetData {
         let conferenceId = super.rawData['conferenceId'];
         if (conferenceId === undefined) {
@@ -94,8 +104,8 @@ class ElementWidget extends Widget {
         };
     }
 
-    public getCompleteUrl(params: ITemplateParams): string {
-        return runTemplate(this.templateUrl, {
+    public getCompleteUrl(params: ITemplateParams, asPopout=false): string {
+        return runTemplate(asPopout ? this.popoutTemplateUrl : this.templateUrl, {
             // we need to supply a whole widget to the template, but don't have
             // easy access to the definition the superclass is using, so be sad
             // and gutwrench it.
@@ -109,7 +119,7 @@ class ElementWidget extends Widget {
 
 export class StopGapWidget extends EventEmitter {
     private messaging: ClientWidgetApi;
-    private mockWidget: Widget;
+    private mockWidget: ElementWidget;
     private scalarToken: string;
 
     constructor(private appTileProps: IAppTileProps) {
@@ -133,12 +143,23 @@ export class StopGapWidget extends EventEmitter {
      * The URL to use in the iframe
      */
     public get embedUrl(): string {
+        return this.runUrlTemplate({asPopout: false});
+    }
+
+    /**
+     * The URL to use in the popout
+     */
+    public get popoutUrl(): string {
+        return this.runUrlTemplate({asPopout: true});
+    }
+
+    private runUrlTemplate(opts = {asPopout: false}): string {
         const templated = this.mockWidget.getCompleteUrl({
             currentRoomId: RoomViewStore.getRoomId(),
             currentUserId: MatrixClientPeg.get().getUserId(),
             userDisplayName: OwnProfileStore.instance.displayName,
             userHttpAvatarUrl: OwnProfileStore.instance.getHttpAvatarUrl(),
-        });
+        }, opts?.asPopout);
 
         // Add in some legacy support sprinkles
         // TODO: Replace these with proper widget params
@@ -158,19 +179,6 @@ export class StopGapWidget extends EventEmitter {
         return parsed.toString().replace(/%24/g, '$');
     }
 
-    /**
-     * The URL to use in the popout
-     */
-    public get popoutUrl(): string {
-        if (WidgetType.JITSI.matches(this.mockWidget.type)) {
-            return WidgetUtils.getLocalJitsiWrapperUrl({
-                forLocalRender: false,
-                auth: this.mockWidget.rawData?.auth,
-            });
-        }
-        return this.embedUrl;
-    }
-
     public get isManagedByManager(): boolean {
         return !!this.scalarToken;
     }
@@ -275,8 +283,8 @@ export class StopGapWidget extends EventEmitter {
         }
     }
 
-    public stop() {
-        if (ActiveWidgetStore.getPersistentWidgetId() === this.mockWidget.id) {
+    public stop(opts = {forceDestroy: false}) {
+        if (!opts?.forceDestroy && ActiveWidgetStore.getPersistentWidgetId() === this.mockWidget.id) {
             console.log("Skipping destroy - persistent widget");
             return;
         }