diff --git a/res/css/views/rooms/_AppsDrawer.scss b/res/css/views/rooms/_AppsDrawer.scss
index 61da3a360b..3a33b73ec9 100644
--- a/res/css/views/rooms/_AppsDrawer.scss
+++ b/res/css/views/rooms/_AppsDrawer.scss
@@ -16,9 +16,10 @@ limitations under the License.
 */
 
 /*
- Minimum size for usual AppTiles and fixed size for mini-tiles.
+ Size settings
 */
-$AppTileMinHeight: 300px;
+$AppsDrawerMinHeight: 50px;
+$AppsDrawerDefaultHeight: 300px;
 $MiniAppTileHeight: 114px;
 
 .mx_AppsDrawer {
@@ -35,6 +36,13 @@ $MiniAppTileHeight: 114px;
     flex-direction: row;
     align-items: stretch;
     justify-content: center;
+    min-height: $AppsDrawerMinHeight;
+    height: $AppsDrawerDefaultHeight;
+}
+
+.mx_AppsDrawer_minimised .mx_AppsContainer {
+    min-height: inherit;
+    height: inherit;
 }
 
 .mx_AddWidget_button {
@@ -67,7 +75,6 @@ $MiniAppTileHeight: 114px;
     border-radius: 4px;
     display: flex;
     flex-direction: column;
-    min-height: $AppTileMinHeight;
 }
 
 .mx_AppTile:last-child {
@@ -83,7 +90,6 @@ $MiniAppTileHeight: 114px;
     border-radius: 4px;
     display: flex;
     flex-direction: column;
-    min-height: $AppTileMinHeight;
 }
 
 .mx_AppTile_mini {
@@ -378,3 +384,27 @@ form.mx_Custom_Widget_Form div {
 .mx_AppLoading iframe {
     display: none;
 }
+
+/* Hidden resize handle (Apptile bottom serves as indicator) */
+.mx_AppsDrawer .mx_ResizeHandle > div {
+    background: inherit;
+}
+
+.mx_AppsDrawer_fullWidth .mx_ResizeHandle {
+    max-width: 960px;
+    margin-left: auto;
+    margin-right: auto;
+}
+
+.mx_AppsDrawer_minimised .mx_ResizeHandle {
+    display: none;
+}
+
+/* Avoid apptile iframes capturing mouse event focus when resizing */
+.mx_AppsDrawer_resizing iframe {
+    pointer-events: none;
+}
+
+.mx_AppsDrawer_resizing .mx_AppTile_persistedWrapper {
+    z-index: 1;
+}
diff --git a/src/components/views/rooms/AppsDrawer.js b/src/components/views/rooms/AppsDrawer.js
index b64eb33435..842b93170f 100644
--- a/src/components/views/rooms/AppsDrawer.js
+++ b/src/components/views/rooms/AppsDrawer.js
@@ -30,6 +30,9 @@ import WidgetEchoStore from "../../../stores/WidgetEchoStore";
 import AccessibleButton from '../elements/AccessibleButton';
 import {IntegrationManagers} from "../../../integrations/IntegrationManagers";
 import SettingsStore from "../../../settings/SettingsStore";
+import classNames from 'classnames';
+import ResizeHandle from '../elements/ResizeHandle';
+import {Resizer, FixedDistributor} from '../../../resizer';
 
 // The maximum number of widgets that can be added in a room
 const MAX_WIDGETS = 2;
@@ -60,6 +63,7 @@ export default createReactClass({
         MatrixClientPeg.get().on('RoomState.events', this.onRoomStateEvents);
         WidgetEchoStore.on('update', this._updateApps);
         this.dispatcherRef = dis.register(this.onAction);
+        this._createResizer();
     },
 
     componentWillUnmount: function() {
@@ -69,6 +73,10 @@ export default createReactClass({
         }
         WidgetEchoStore.removeListener('update', this._updateApps);
         if (this.dispatcherRef) dis.unregister(this.dispatcherRef);
+        if (this.resizer) {
+            this.resizer.detach();
+            this.resizer = null;
+        }
     },
 
     // TODO: [REACT-WARNING] Replace with appropriate lifecycle event
@@ -154,6 +162,30 @@ export default createReactClass({
         this._launchManageIntegrations();
     },
 
+    _createResizer: function() {
+        if (!this.resizeContainer) {
+            return;
+        }
+
+        const classNames = {
+            handle: "mx_ResizeHandle",
+            vertical: "mx_ResizeHandle_vertical",
+            resizing: "mx_AppsDrawer_resizing",
+        };
+        const resizer = new Resizer(
+            this.resizeContainer,
+            FixedDistributor,
+            {},
+        );
+        resizer.setClassNames(classNames);
+        resizer.attach();
+        this.resizer = resizer;
+    },
+
+    _setResizeContainerRef: function(div) {
+        this.resizeContainer = div;
+    },
+
     render: function() {
         const apps = this.state.apps.map((app, index, arr) => {
             const capWhitelist = WidgetUtils.getCapWhitelistForAppTypeInRoomId(app.type, this.props.room.roomId);
@@ -191,6 +223,13 @@ export default createReactClass({
             </AccessibleButton>;
         }
 
+        const containerStyle = {
+            maxHeight: Math.max(this.props.maxHeight - 50, 300),
+        };
+        if (!this.props.showApps && this.resizer) {
+            this.resizer.forHandleAt(0).item.clearSize();
+        }
+
         let spinner;
         if (
             apps.length === 0 && WidgetEchoStore.roomHasPendingWidgets(
@@ -202,12 +241,20 @@ export default createReactClass({
             spinner = <Loader />;
         }
 
+        const classes = classNames({
+            "mx_AppsDrawer": true,
+            "mx_AppsDrawer_hidden": this.props.hide,
+            "mx_AppsDrawer_fullWidth": apps.length < 2,
+            "mx_AppsDrawer_minimised": !this.props.showApps,
+        });
+
         return (
-            <div className={'mx_AppsDrawer' + (this.props.hide ? ' mx_AppsDrawer_hidden' : '')}>
-                <div id='apps' className='mx_AppsContainer'>
+            <div className={classes} ref={this._setResizeContainerRef}>
+                <div id='apps' className='mx_AppsContainer' style={containerStyle}>
                     { apps }
                     { spinner }
                 </div>
+                <ResizeHandle vertical={true} />
                 { this._canUserModify() && addWidget }
             </div>
         );