diff --git a/crates/egui/src/containers/area.rs b/crates/egui/src/containers/area.rs
index 4b3a4f722..61375b580 100644
--- a/crates/egui/src/containers/area.rs
+++ b/crates/egui/src/containers/area.rs
@@ -454,14 +454,12 @@ impl Area {
             state.size = None;
         }
         state.pivot = pivot;
-        state.interactable = interactable;
         if let Some(new_pos) = new_pos {
             state.pivot_pos = Some(new_pos);
         }
         state.pivot_pos.get_or_insert_with(|| {
             default_pos.unwrap_or_else(|| automatic_area_position(ctx, constrain_rect, layer_id))
         });
-        state.interactable = interactable;
 
         let size = *state.size.get_or_insert_with(|| {
             sizing_pass = true;
@@ -484,6 +482,10 @@ impl Area {
             size
         });
 
+        // We should never be interactable during a sizing pass, since then we are shown at a different
+        // size which might interfere with hover state of the hovered widget causing popup feedback loops.
+        state.interactable = interactable && !sizing_pass;
+
         // TODO(emilk): if last frame was sizing pass, it should be considered invisible for smoother fade-in
         let visible_last_frame = ctx.memory(|mem| mem.areas().visible_last_frame(&layer_id));
 
diff --git a/crates/egui/src/containers/popup.rs b/crates/egui/src/containers/popup.rs
index 080c00bd1..587c77e23 100644
--- a/crates/egui/src/containers/popup.rs
+++ b/crates/egui/src/containers/popup.rs
@@ -180,6 +180,7 @@ pub struct Popup<'a> {
     /// Default width passed to the Area
     width: Option<f32>,
     sense: Sense,
+    interactable: bool,
     layout: Layout,
     frame: Option<Frame>,
     style: StyleModifier,
@@ -202,6 +203,7 @@ impl<'a> Popup<'a> {
             gap: 0.0,
             width: None,
             sense: Sense::click(),
+            interactable: true,
             layout: Layout::default(),
             frame: None,
             style: StyleModifier::default(),
@@ -369,6 +371,15 @@ impl<'a> Popup<'a> {
         self
     }
 
+    /// If `false`, the pointer goes straight through the popup and it's widgets to whatever is behind it.
+    ///
+    /// Default: `true`.
+    #[inline]
+    pub fn interactable(mut self, interactable: bool) -> Self {
+        self.interactable = interactable;
+        self
+    }
+
     /// Set the sense of the popup.
     #[inline]
     pub fn sense(mut self, sense: Sense) -> Self {
@@ -546,6 +557,7 @@ impl<'a> Popup<'a> {
             gap,
             width,
             sense,
+            interactable,
             layout,
             frame,
             style,
@@ -570,6 +582,7 @@ impl<'a> Popup<'a> {
             .pivot(pivot)
             .fixed_pos(anchor)
             .sense(sense)
+            .interactable(interactable)
             .layout(layout)
             .sizing_pass(!was_open_last_frame)
             .info(info.unwrap_or_else(|| {
diff --git a/crates/egui/src/containers/tooltip.rs b/crates/egui/src/containers/tooltip.rs
index 22c319569..a372d6cd1 100644
--- a/crates/egui/src/containers/tooltip.rs
+++ b/crates/egui/src/containers/tooltip.rs
@@ -129,7 +129,15 @@ impl Tooltip<'_> {
         });
 
         let tooltip_area_id = Self::tooltip_id(parent_widget, state.tooltip_count);
-        popup = popup.anchor(state.bounding_rect).id(tooltip_area_id);
+
+        // Tooltips without interactive contents should not be interactable (hover should pass
+        // through to the widget below).
+        let interactable = Self::had_interactive_widgets(popup.ctx(), tooltip_area_id);
+
+        popup = popup
+            .anchor(state.bounding_rect)
+            .id(tooltip_area_id)
+            .interactable(interactable);
 
         let response = popup.show(|ui| {
             // By default, the text in tooltips aren't selectable.
@@ -192,6 +200,20 @@ impl Tooltip<'_> {
         widget_id.with(tooltip_count)
     }
 
+    /// Did this tooltip contain anything the user can interact with, last pass?
+    ///
+    /// Most tooltips are just text. Those should not react to the pointer at all,
+    /// or they would steal the hover from the widget they belong to.
+    fn had_interactive_widgets(ctx: &Context, tooltip_id: Id) -> bool {
+        let tooltip_layer_id = LayerId::new(Order::Tooltip, tooltip_id);
+        ctx.viewport(|vp| {
+            vp.prev_pass
+                .widgets
+                .get_layer(tooltip_layer_id)
+                .any(|w| w.enabled && w.sense.interactive())
+        })
+    }
+
     /// Should we show a tooltip for this response?
     ///
     /// Argument `allow_interactive_tooltip` controls whether mouse can interact with tooltip that
@@ -247,15 +269,9 @@ impl Tooltip<'_> {
             // Check if we should automatically stay open:
 
             let tooltip_id = Self::next_tooltip_id(&response.ctx, response.id);
-            let tooltip_layer_id = LayerId::new(Order::Tooltip, tooltip_id);
 
             let tooltip_has_interactive_widget = allow_interactive_tooltip
-                && response.ctx.viewport(|vp| {
-                    vp.prev_pass
-                        .widgets
-                        .get_layer(tooltip_layer_id)
-                        .any(|w| w.enabled && w.sense.interactive())
-                });
+                && Self::had_interactive_widgets(&response.ctx, tooltip_id);
 
             if tooltip_has_interactive_widget {
                 // We keep the tooltip open if hovered,
diff --git a/crates/egui/src/context.rs b/crates/egui/src/context.rs
index 78f6ead11..e0705b201 100644
--- a/crates/egui/src/context.rs
+++ b/crates/egui/src/context.rs
@@ -466,7 +466,13 @@ impl ContextImpl {
         viewport.this_pass.begin_pass();
 
         {
-            let mut layers: Vec<LayerId> = viewport.prev_pass.widgets.layer_ids().collect();
+            // Areas that are not interactable are click-through: skip them in the hit-test.
+            let mut layers: Vec<LayerId> = viewport
+                .prev_pass
+                .widgets
+                .layer_ids()
+                .filter(|layer_id| self.memory.areas().is_interactable(*layer_id))
+                .collect();
             layers.sort_by(|&a, &b| self.memory.areas().compare_order(a, b));
 
             viewport.hits = if let Some(pos) = viewport.input.pointer.interact_pos() {
diff --git a/crates/egui/src/memory/mod.rs b/crates/egui/src/memory/mod.rs
index 1f22b3dd4..8fd407cc9 100644
--- a/crates/egui/src/memory/mod.rs
+++ b/crates/egui/src/memory/mod.rs
@@ -1194,6 +1194,11 @@ impl Areas {
         self.areas.get_mut(&id)
     }
 
+    /// Can the user interact with this layer or it's widgets, or do clicks go straight through it?
+    pub(crate) fn is_interactable(&self, layer_id: LayerId) -> bool {
+        self.get(layer_id.id).is_none_or(|area| area.interactable)
+    }
+
     /// All layers back-to-front, top is last.
     pub(crate) fn order(&self) -> &[LayerId] {
         &self.order
diff --git a/tests/egui_tests/tests/regression_tests.rs b/tests/egui_tests/tests/regression_tests.rs
index f250b1ab2..34527f4cc 100644
--- a/tests/egui_tests/tests/regression_tests.rs
+++ b/tests/egui_tests/tests/regression_tests.rs
@@ -1,15 +1,15 @@
 use std::sync::Arc;
 
-use egui::ScrollArea;
 use egui::accesskit::Role;
 #[cfg(debug_assertions)]
 use egui::epaint::Shape;
 use egui::style::ScrollAnimation;
 use egui::text::{LayoutJob, TextWrapping};
 use egui::{
-    Align, Button, Color32, FontFamily, FontId, Image, Label, Layout, RichText, Sense, TextBuffer,
-    TextFormat, TextWrapMode, Ui, include_image, vec2,
+    Align, Button, Color32, FontFamily, FontId, Image, Label, Layout, Rect, RichText, Sense,
+    TextBuffer, TextFormat, TextWrapMode, Ui, Vec2, include_image, vec2,
 };
+use egui::{Pos2, ScrollArea};
 use egui_kittest::Harness;
 use egui_kittest::kittest::{NodeT as _, Queryable as _};
 
@@ -481,3 +481,81 @@ fn animated_scroll_beats_sticky_bottom() {
         "animated explicit scroll should leave the sticky bottom"
     );
 }
+
+/// Tests that tooltips are shown correctly for buttons that are only shown on hover.
+///
+/// Basically, this tests that a tooltip overlapping the mouse cursor does not interfere with a
+/// buttons hover state.
+#[test]
+fn tooltip_should_work_for_hover_button() {
+    let button_rect = Rect::from_min_size(Pos2::new(4.0, 4.0), Vec2::new(80.0, 20.0));
+    let mut harness = Harness::builder().with_size((320.0, 80.0)).build_ui(|ui| {
+        if ui.rect_contains_pointer(button_rect) {
+            ui.button("A tooltip should be shown")
+                .on_hover_text("My tooltip");
+        }
+    });
+
+    harness.hover_at(button_rect.center());
+
+    harness.run();
+
+    harness.snapshot("test_tooltip_hover_regression");
+}
+
+/// Ensure that hovering close to a widget doesn't cause a tooltip feedback loop (due to a
+/// difference between `hovered` and `contains_pointer` caused by the interact radius).
+#[test]
+fn tooltip_covering_button_should_not_cause_feedback_loop() {
+    let mut harness = Harness::builder().with_size((200.0, 30.0)).build_ui(|ui| {
+        ui.button("A tooltip should be shown")
+            .on_hover_text("This tooltip is larger than the button");
+    });
+
+    harness.hover_at(
+        harness
+            .get_by_label("A tooltip should be shown")
+            .rect()
+            .left_center()
+            - Vec2::X,
+    );
+
+    harness.run();
+
+    harness.snapshot("tooltip_covering_button_should_not_cause_feedback_loop");
+}
+
+/// Tests that a tooltip closes when the pointer moves onto a neighboring widget,
+/// so that the neighbor can show its own tooltip.
+///
+/// The two buttons are only `item_spacing.y` (3 pt) apart, which is less than the
+/// hit-test `interact_radius` (5 pt), so the first button is still close enough to
+/// interact with when the pointer is on the second one.
+#[test]
+fn tooltip_should_hand_over_to_neighboring_widget() {
+    let mut harness = Harness::builder().with_size((300.0, 200.0)).build_ui(|ui| {
+        ui.button("Button A").on_hover_text("Tooltip A");
+        ui.button("Button B").on_hover_text("Tooltip B");
+    });
+
+    let a_rect = harness.get_by_label("Button A").rect();
+    let b_rect = harness.get_by_label("Button B").rect();
+
+    harness.hover_at(a_rect.center_bottom() - Vec2::Y);
+    harness.run();
+    assert!(
+        harness.query_by_label("Tooltip A").is_some(),
+        "Tooltip A should be shown when hovering Button A"
+    );
+
+    harness.hover_at(b_rect.center_top() + Vec2::Y);
+    harness.run();
+    assert!(
+        harness.query_by_label("Tooltip B").is_some(),
+        "Tooltip B should be shown when hovering Button B"
+    );
+    assert!(
+        harness.query_by_label("Tooltip A").is_none(),
+        "Tooltip A should be hidden when hovering Button B"
+    );
+}
diff --git a/tests/egui_tests/tests/snapshots/test_tooltip_hover_regression.png b/tests/egui_tests/tests/snapshots/test_tooltip_hover_regression.png
new file mode 100644
index 000000000..9f489aa81
--- /dev/null
+++ b/tests/egui_tests/tests/snapshots/test_tooltip_hover_regression.png
@@ -0,0 +1,3 @@
+version https://git-lfs.github.com/spec/v1
+oid sha256:59bef0e3593896985988c03171c710d8ed31ed8bb89c7a3f63c060c573e4fb74
+size 6510
diff --git a/tests/egui_tests/tests/snapshots/tooltip_covering_button_should_not_cause_feedback_loop.png b/tests/egui_tests/tests/snapshots/tooltip_covering_button_should_not_cause_feedback_loop.png
new file mode 100644
index 000000000..53f8ff24d
--- /dev/null
+++ b/tests/egui_tests/tests/snapshots/tooltip_covering_button_should_not_cause_feedback_loop.png
@@ -0,0 +1,3 @@
+version https://git-lfs.github.com/spec/v1
+oid sha256:ed2f80921ab864b0df3303834a8ab943a3aa5e10456896991c2dca81be0c4968
+size 3968