diff --git a/input.h b/input.h
--- a/input.h
+++ b/input.h
@@ -381,7 +381,7 @@
      * @return Toplevel* at device position.
      **/
     QPointer<Toplevel> at() const {
-        return m_at;
+        return m_at.at;
     }
     /**
      * @brief Toplevel currently having pointer input focus (this might
@@ -451,7 +451,11 @@
 
     QWindow* findInternalWindow(const QPoint &pos) const;
 
-    QPointer<Toplevel> m_at;
+    struct {
+        QPointer<Toplevel> at;
+        QMetaObject::Connection surfaceCreatedConnection;
+    } m_at;
+
     struct {
         QPointer<Toplevel> focus;
         QPointer<Decoration::DecoratedClientImpl> decoration;
diff --git a/input.cpp b/input.cpp
--- a/input.cpp
+++ b/input.cpp
@@ -2229,11 +2229,14 @@
 
 bool InputDeviceHandler::setAt(Toplevel *toplevel)
 {
-    if (m_at == toplevel) {
+    if (m_at.at == toplevel) {
         return false;
     }
-    auto old = m_at;
-    m_at = toplevel;
+    auto old = m_at.at;
+    disconnect(m_at.surfaceCreatedConnection);
+    m_at.surfaceCreatedConnection = QMetaObject::Connection();
+
+    m_at.at = toplevel;
     emit atChanged(old, toplevel);
     return true;
 }
@@ -2261,16 +2264,26 @@
 void InputDeviceHandler::updateFocus()
 {
     auto oldFocus = m_focus.focus;
-    m_focus.focus = m_at;
+
+    if (m_at.at && !m_at.at->surface()) {
+        if (!m_at.surfaceCreatedConnection) {
+            m_at.surfaceCreatedConnection = connect(m_at.at, &Toplevel::surfaceChanged,
+                                                    this, &InputDeviceHandler::update);
+        }
+        m_focus.focus = nullptr;
+    } else {
+        m_focus.focus = m_at.at;
+    }
+
     focusUpdate(oldFocus, m_focus.focus);
 }
 
 bool InputDeviceHandler::updateDecoration()
 {
     const auto oldDeco = m_focus.decoration;
     m_focus.decoration = nullptr;
 
-    auto *ac = qobject_cast<AbstractClient*>(m_at);
+    auto *ac = qobject_cast<AbstractClient*>(m_at.at);
     if (ac && ac->decoratedClient()) {
         const QRect clientRect = QRect(ac->clientPos(), ac->clientSize()).translated(ac->pos());
         if (!clientRect.contains(position().toPoint())) {
@@ -2338,7 +2351,7 @@
     }
     updateInternalWindow(nullptr);
 
-    if (m_focus.focus != m_at) {
+    if (m_focus.focus != m_at.at) {
         // focus change
         updateDecoration();
         updateFocus();