diff --git a/res/css/views/rooms/_AppsDrawer.scss b/res/css/views/rooms/_AppsDrawer.scss
index 8731d22660..492ed95973 100644
--- a/res/css/views/rooms/_AppsDrawer.scss
+++ b/res/css/views/rooms/_AppsDrawer.scss
@@ -24,26 +24,45 @@ $MiniAppTileHeight: 200px;
     flex-direction: column;
     overflow: hidden;
 
+    .mx_AppsContainer_resizerHandleContainer {
+        width: 100%;
+        height: 10px;
+        margin-top: -3px; // move it up so the interactions are slightly more comfortable
+        display: block;
+        position: relative;
+    }
+
     .mx_AppsContainer_resizerHandle {
         cursor: ns-resize;
-        border-radius: 3px;
 
-        // Override styles from library
-        width: unset !important;
-        height: 4px !important;
+        // Override styles from library, making the whole area the target area
+        width: 100% !important;
+        height: 100% !important;
 
         // This is positioned directly below frame
         position: absolute;
-        bottom: -8px !important; // override from library
+        bottom: 0 !important; // override from library
 
-        // Together, these make the bar 64px wide
-        // These are also overridden from the library
-        left: calc(50% - 32px) !important;
-        right: calc(50% - 32px) !important;
+        // We then render the pill handle in an ::after to keep it in the handle's
+        // area without being a massive line across the screen
+        &::after {
+            content: '';
+            position: absolute;
+            border-radius: 3px;
+
+            // The combination of these two should make the pill 4px high
+            top: 6px;
+            bottom: 0;
+
+            // Together, these make the bar 64px wide
+            // These are also overridden from the library
+            left: calc(50% - 32px);
+            right: calc(50% - 32px);
+        }
     }
 
     &:hover {
-        .mx_AppsContainer_resizerHandle {
+        .mx_AppsContainer_resizerHandle::after {
             opacity: 0.8;
             background: $primary-fg-color;
         }
diff --git a/src/components/views/rooms/AppsDrawer.js b/src/components/views/rooms/AppsDrawer.js
index 3208844bc5..24a7d1417a 100644
--- a/src/components/views/rooms/AppsDrawer.js
+++ b/src/components/views/rooms/AppsDrawer.js
@@ -252,6 +252,7 @@ export default class AppsDrawer extends React.Component {
                     minHeight={100}
                     maxHeight={this.props.maxHeight ? this.props.maxHeight - 50 : undefined}
                     handleClass="mx_AppsContainer_resizerHandle"
+                    handleWrapperClass="mx_AppsContainer_resizerHandleContainer"
                     className="mx_AppsContainer_resizer"
                     resizeNotifier={this.props.resizeNotifier}
                 >