diff --git a/interface/src/Application.cpp b/interface/src/Application.cpp
index 37c3b361bf..26da43fb58 100644
--- a/interface/src/Application.cpp
+++ b/interface/src/Application.cpp
@@ -921,17 +921,10 @@ Application::Application(int& argc, char** argv, QElapsedTimer& startupTimer) :
                 cycleCamera();
             } else if (action == controller::toInt(controller::Action::UI_NAV_SELECT)) {
                 if (!offscreenUi->navigationFocused()) {
-                    auto reticlePosition = getApplicationCompositor().getReticlePosition();
-                    offscreenUi->toggleMenu(QPoint(reticlePosition.x, reticlePosition.y));
+                    toggleMenuUnderReticle();
                 }
             } else if (action == controller::toInt(controller::Action::CONTEXT_MENU)) {
-                auto reticlePosition = getApplicationCompositor().getReticlePosition();
-                offscreenUi->toggleMenu(QPoint(reticlePosition.x, reticlePosition.y));
-            } else if (action == controller::toInt(controller::Action::UI_NAV_SELECT)) {
-                if (!offscreenUi->navigationFocused()) {
-                    auto reticlePosition = getApplicationCompositor().getReticlePosition();
-                    offscreenUi->toggleMenu(QPoint(reticlePosition.x, reticlePosition.y));
-                }
+                toggleMenuUnderReticle();
             } else if (action == controller::toInt(controller::Action::RETICLE_X)) {
                 auto oldPos = getApplicationCompositor().getReticlePosition();
                 getApplicationCompositor().setReticlePosition({ oldPos.x + state, oldPos.y });
@@ -1240,7 +1233,16 @@ QString Application::getUserAgent() {
     return userAgent;
 }
 
-
+void Application::toggleMenuUnderReticle() const {
+    // In HMD, if the menu is near the mouse but not under it, the reticle can be at a significantly
+    // different depth. When you focus on the menu, the cursor can appear to your crossed eyes as both
+    // on the menu and off.
+    // Even in 2D, it is arguable whether the user would want the menu to be to the side.
+    const float X_LEFT_SHIFT = 50.0;
+    auto offscreenUi = DependencyManager::get<OffscreenUi>();
+    auto reticlePosition = getApplicationCompositor().getReticlePosition();
+    offscreenUi->toggleMenu(QPoint(reticlePosition.x - X_LEFT_SHIFT, reticlePosition.y));
+}
 
 void Application::checkChangeCursor() {
     QMutexLocker locker(&_changeCursorLock);
@@ -2462,9 +2464,7 @@ void Application::keyPressEvent(QKeyEvent* event) {
 
 void Application::keyReleaseEvent(QKeyEvent* event) {
     if (event->key() == Qt::Key_Alt && _altPressed && hasFocus()) {
-        auto offscreenUi = DependencyManager::get<OffscreenUi>();
-        auto reticlePosition = getApplicationCompositor().getReticlePosition();
-        offscreenUi->toggleMenu(QPoint(reticlePosition.x, reticlePosition.y));
+        toggleMenuUnderReticle();
     }
 
     _keysPressed.remove(event->key());
diff --git a/interface/src/Application.h b/interface/src/Application.h
index 5beaa5b455..6857ba2a3a 100644
--- a/interface/src/Application.h
+++ b/interface/src/Application.h
@@ -408,6 +408,7 @@ private:
     static void dragEnterEvent(QDragEnterEvent* event);
 
     void maybeToggleMenuVisible(QMouseEvent* event) const;
+    void toggleMenuUnderReticle() const;
 
     MainWindow* _window;
     QElapsedTimer& _sessionRunTimer;
diff --git a/libraries/ui/src/OffscreenUi.cpp b/libraries/ui/src/OffscreenUi.cpp
index fa1a31d196..1a7d4b2328 100644
--- a/libraries/ui/src/OffscreenUi.cpp
+++ b/libraries/ui/src/OffscreenUi.cpp
@@ -492,10 +492,9 @@ void OffscreenUi::unfocusWindows() {
     Q_ASSERT(invokeResult);
 }
 
-void OffscreenUi::toggleMenu(const QPoint& screenPosition) {
+void OffscreenUi::toggleMenu(const QPoint& screenPosition) { // caller should already have mapped using getReticlePosition
     emit showDesktop(); // we really only want to do this if you're showing the menu, but for now this works
-    auto virtualPos = mapToVirtualScreen(screenPosition, nullptr);
-    QMetaObject::invokeMethod(_desktop, "toggleMenu",  Q_ARG(QVariant, virtualPos));
+    QMetaObject::invokeMethod(_desktop, "toggleMenu", Q_ARG(QVariant, screenPosition));
 }
 
 
diff --git a/scripts/system/controllers/handControllerPointer.js b/scripts/system/controllers/handControllerPointer.js
index 374be0d1a1..a0f1f47b3c 100644
--- a/scripts/system/controllers/handControllerPointer.js
+++ b/scripts/system/controllers/handControllerPointer.js
@@ -208,9 +208,9 @@ function isShakingMouse() { // True if the person is waving the mouse around try
     return isShaking;
 }
 var NON_LINEAR_DIVISOR = 2;
-var MINIMUM_SEEK_DISTANCE = 0.01;
-function updateSeeking() {
-    if (!Reticle.visible || isShakingMouse()) {
+var MINIMUM_SEEK_DISTANCE = 0.1;
+function updateSeeking(doNotStartSeeking) {
+    if (!doNotStartSeeking && (!Reticle.visible || isShakingMouse())) {
         if (!isSeeking) {
             print('Start seeking mouse.');
             isSeeking = true;
@@ -224,8 +224,8 @@ function updateSeeking() {
     if (!lookAt2D) { // If this happens, something has gone terribly wrong.
         print('Cannot seek without lookAt position');
         isSeeking = false;
-        return;
-    } // E.g., if parallel to location in HUD
+        return; // E.g., if parallel to location in HUD
+    }
     var copy = Reticle.position;
     function updateDimension(axis) {
         var distanceBetween = lookAt2D[axis] - Reticle.position[axis];
@@ -353,6 +353,16 @@ clickMapping.from(rightTrigger.full).when(isPointingAtOverlayStartedNonFullTrigg
 clickMapping.from(leftTrigger.full).when(isPointingAtOverlayStartedNonFullTrigger(leftTrigger)).to(Controller.Actions.ReticleClick);
 clickMapping.from(Controller.Standard.RightSecondaryThumb).peek().to(Controller.Actions.ContextMenu);
 clickMapping.from(Controller.Standard.LeftSecondaryThumb).peek().to(Controller.Actions.ContextMenu);
+clickMapping.from(Controller.Hardware.Keyboard.RightMouseClicked).peek().to(function () {
+    // Allow the reticle depth to be set correctly:
+    // Wait a tick for the context menu to be displayed, and then simulate a (non-hand-controller) mouse move
+    // so that the system updates qml state (Reticle.pointingAtSystemOverlay) before it gives us a mouseMove.
+    // We don't want the system code to always do this for us, because, e.g., we do not want to get a mouseMove
+    // after the Left/RightSecondaryThumb gives us a context menu. Only from the mouse.
+    Script.setTimeout(function () {
+        Reticle.setPosition(Reticle.position);
+    }, 0);
+});
 // Partial smoothed trigger is activation.
 clickMapping.from(rightTrigger.partial).to(makeToggleAction(Controller.Standard.RightHand));
 clickMapping.from(leftTrigger.partial).to(makeToggleAction(Controller.Standard.LeftHand));
@@ -386,6 +396,7 @@ function update() {
         expireMouseCursor();
         clearSystemLaser();
     }
+    updateSeeking(true);
     if (!handControllerLockOut.expired(now)) {
         return off(); // Let them use mouse it in peace.
     }