diff --git a/crates/egui/src/containers/popup.rs b/crates/egui/src/containers/popup.rs
index 105f4a5b32e..ab01aa6ab30 100644
--- a/crates/egui/src/containers/popup.rs
+++ b/crates/egui/src/containers/popup.rs
@@ -124,7 +124,12 @@ fn show_tooltip_at_dyn<'c, R>(
     }
 
     // if there are multiple tooltips open they should use the same common_id for the `tooltip_size` caching to work.
-    let mut state = ctx.frame_state(|fs| {
+    let mut state = ctx.frame_state_mut(|fs| {
+        // Remember that this is the widget showing the tooltip:
+        fs.tooltip_state
+            .per_layer_tooltip_widget
+            .insert(parent_layer, widget_id);
+
         fs.tooltip_state
             .widget_tooltips
             .get(&widget_id)
diff --git a/crates/egui/src/frame_state.rs b/crates/egui/src/frame_state.rs
index 4e1aa390017..4f434a60ebc 100644
--- a/crates/egui/src/frame_state.rs
+++ b/crates/egui/src/frame_state.rs
@@ -1,13 +1,27 @@
 use crate::{id::IdSet, *};
 
+/// Reset at the start of each frame.
 #[derive(Clone, Debug, Default)]
 pub struct TooltipFrameState {
+    /// If a tooltip has been shown this frame, where was it?
+    /// This is used to prevent multiple tooltips to cover each other.
     pub widget_tooltips: IdMap<PerWidgetTooltipState>,
+
+    /// For each layer, which widget is showing a tooltip (if any)?
+    ///
+    /// Only one widget per layer may show a tooltip.
+    /// But if a tooltip contains a tooltip, you can show a tooltip on top of a tooltip.
+    pub per_layer_tooltip_widget: ahash::HashMap<LayerId, Id>,
 }
 
 impl TooltipFrameState {
     pub fn clear(&mut self) {
-        self.widget_tooltips.clear();
+        let Self {
+            widget_tooltips,
+            per_layer_tooltip_widget,
+        } = self;
+        widget_tooltips.clear();
+        per_layer_tooltip_widget.clear();
     }
 }
 
@@ -51,9 +65,6 @@ pub struct FrameState {
     /// How much space is used by panels.
     pub used_by_panels: Rect,
 
-    /// If a tooltip has been shown this frame, where was it?
-    /// This is used to prevent multiple tooltips to cover each other.
-    /// Reset at the start of each frame.
     pub tooltip_state: TooltipFrameState,
 
     /// The current scroll area should scroll to this range (horizontal, vertical).
diff --git a/crates/egui/src/response.rs b/crates/egui/src/response.rs
index e2d898dae1a..f0f10b9d4c1 100644
--- a/crates/egui/src/response.rs
+++ b/crates/egui/src/response.rs
@@ -645,6 +645,22 @@ impl Response {
             }
         }
 
+        let is_other_tooltip_open = self.ctx.prev_frame_state(|fs| {
+            if let Some(already_open_tooltip) = fs
+                .tooltip_state
+                .per_layer_tooltip_widget
+                .get(&self.layer_id)
+            {
+                already_open_tooltip != &self.id
+            } else {
+                false
+            }
+        });
+        if is_other_tooltip_open {
+            // We only allow one tooltip per layer. First one wins. It is up to that tooltip to close itself.
+            return false;
+        }
+
         // Fast early-outs:
         if self.enabled {
             if !self.hovered || !self.ctx.input(|i| i.pointer.has_pointer()) {