diff --git a/Libraries/LibWeb/DOM/Node.cpp b/Libraries/LibWeb/DOM/Node.cpp
index a52755195ab23..ec2ce7d2327b4 100644
--- a/Libraries/LibWeb/DOM/Node.cpp
+++ b/Libraries/LibWeb/DOM/Node.cpp
@@ -1686,12 +1686,24 @@ void Node::recompute_editable_subtree_flags_and_repaint()
         // display list, so a flip must invalidate the recorded output.
         if (node.recompute_editable_subtree_flag())
             node.set_needs_repaint();
-        // Editing-host status is stamped into layout NodeData at layout node construction;
-        // contenteditable and designMode changes reach here without a layout tree rebuild,
-        // so the stamp must be refreshed. A node's editing-host status can flip even when
-        // its own editable-subtree flag did not, hence unconditionally for every node.
-        if (auto* layout_node = node.unsafe_layout_node())
-            layout_node->set_is_editing_host(node.is_editing_host());
+        // Editing-host status and the empty-text fragment behavior of text nodes are
+        // stamped into layout NodeData at layout node construction; contenteditable and
+        // designMode changes reach here without a layout tree rebuild, so the stamps must
+        // be refreshed. A node's stamps can flip even when its own editable-subtree flag
+        // did not, hence unconditionally for every node. A flipped stamp changes geometry
+        // (an editing host gains a minimum block size, an empty editable text node gains
+        // a zero-width fragment), so the affected node also needs a relayout.
+        if (auto* layout_node = node.unsafe_layout_node()) {
+            auto is_editing_host = node.is_editing_host();
+            if (layout_node->is_editing_host() != is_editing_host) {
+                layout_node->set_is_editing_host(is_editing_host);
+                node.set_needs_layout_update(SetNeedsLayoutReason::EditableStateChange);
+            }
+            if (auto* layout_text_node = as_if<Layout::TextNode>(*layout_node)) {
+                if (layout_text_node->update_produces_line_box_fragment_when_empty_flag())
+                    node.set_needs_layout_update(SetNeedsLayoutReason::EditableStateChange);
+            }
+        }
         return TraversalDecision::Continue;
     });
 }
diff --git a/Libraries/LibWeb/DOM/Node.h b/Libraries/LibWeb/DOM/Node.h
index 3870fd71cf6d6..393fd5bf93c9b 100644
--- a/Libraries/LibWeb/DOM/Node.h
+++ b/Libraries/LibWeb/DOM/Node.h
@@ -67,6 +67,7 @@ enum class ShouldComputeRole {
 
 #define ENUMERATE_SET_NEEDS_LAYOUT_REASONS(X)         \
     X(CharacterDataReplaceData)                       \
+    X(EditableStateChange)                            \
     X(FinalizeACrossDocumentNavigation)               \
     X(GeneratedContentImageFinishedLoading)           \
     X(HTMLCanvasElementWidthOrHeightChange)           \
diff --git a/Libraries/LibWeb/HTML/HTMLInputElement.cpp b/Libraries/LibWeb/HTML/HTMLInputElement.cpp
index 5d7f65da051cd..4a1f158bb3160 100644
--- a/Libraries/LibWeb/HTML/HTMLInputElement.cpp
+++ b/Libraries/LibWeb/HTML/HTMLInputElement.cpp
@@ -1189,7 +1189,7 @@ void HTMLInputElement::create_text_input_shadow_tree()
                 overflow: auto;
                 scrollbar-width: none;
                 text-overflow: clip;
-                white-space: nowrap;
+                white-space: pre;
             )~~~"sv);
         }
         m_inner_text_element->set_inline_style(*style);
diff --git a/Libraries/LibWeb/Layout/LayoutRustBridge.cpp b/Libraries/LibWeb/Layout/LayoutRustBridge.cpp
index 5c3415fd2a1d7..9dc50ab3cc4a8 100644
--- a/Libraries/LibWeb/Layout/LayoutRustBridge.cpp
+++ b/Libraries/LibWeb/Layout/LayoutRustBridge.cpp
@@ -38,12 +38,9 @@
 #include <LibWeb/DOM/Document.h>
 #include <LibWeb/DOM/Element.h>
 #include <LibWeb/DOM/Node.h>
-#include <LibWeb/DOM/Position.h>
-#include <LibWeb/DOM/ShadowRoot.h>
 #include <LibWeb/DOM/Text.h>
 #include <LibWeb/Dump.h>
 #include <LibWeb/HTML/AttributeNames.h>
-#include <LibWeb/HTML/FormAssociatedElement.h>
 #include <LibWeb/HTML/HTMLElement.h>
 #include <LibWeb/HTML/HTMLInputElement.h>
 #include <LibWeb/Layout/Box.h>
@@ -95,23 +92,6 @@ static_assert(to_underlying(CSS::StyleGroupIndex::SizingValues) == RustFFI::STYL
 static_assert(to_underlying(CSS::StyleGroupIndex::SurroundValues) == RustFFI::STYLE_GROUP_INDEX_SURROUND);
 static_assert(to_underlying(CSS::StyleGroupIndex::BoxValues) == RustFFI::STYLE_GROUP_INDEX_BOX);
 
-static bool is_empty_editable_text_node(TextNode const& text_node)
-{
-    if (!text_node.text_for_rendering().is_empty())
-        return false;
-    auto const* dom_text = text_node.dom_text();
-    if (!dom_text)
-        return false;
-
-    auto is_empty_editable = false;
-    if (auto const* shadow_root = as_if<DOM::ShadowRoot>(dom_text->root())) {
-        if (auto const* form_associated_element = as_if<HTML::FormAssociatedTextControlElement>(shadow_root->host()))
-            is_empty_editable = form_associated_element->text_control_to_html_element().is_mutable();
-    }
-    is_empty_editable |= dom_text->parent() && dom_text->parent()->is_editing_host();
-    return is_empty_editable;
-}
-
 static CSS::GridTrackSizeList build_used_grid_track_list(RustFFI::FfiUsedGridTrackList const& list)
 {
     auto result = list.is_subgrid ? CSS::GridTrackSizeList::make_subgrid() : CSS::GridTrackSizeList::make_none();
@@ -1266,16 +1246,6 @@ RustFFI::FfiLayoutFcCallbacks LayoutRustBridge::formatting_context_callbacks()
                 facts.marker_list_style_position = static_cast<u8>(to_underlying(marker->list_style_position()));
             }
             return facts; },
-        .text_node_is_empty_editable = [](void*, void* node) {
-            auto const* text_node = as_if<TextNode>(*static_cast<Node const*>(node));
-            VERIFY(text_node);
-            return is_empty_editable_text_node(*text_node); },
-        .document_cursor_is_on_node = [](void*, void* node) {
-            auto const* dom_node = static_cast<Node const*>(node)->dom_node();
-            if (!dom_node)
-                return false;
-            auto cursor_position = dom_node->document().cursor_position();
-            return cursor_position && cursor_position->node() == dom_node; },
         .build_svg_facts = [](void*, void* node) {
             auto const* node_with_style = as_if<NodeWithStyle>(*static_cast<Node const*>(node));
             VERIFY(node_with_style);
diff --git a/Libraries/LibWeb/Layout/Node.h b/Libraries/LibWeb/Layout/Node.h
index 9f352716353a6..e1fa1c40b1d92 100644
--- a/Libraries/LibWeb/Layout/Node.h
+++ b/Libraries/LibWeb/Layout/Node.h
@@ -262,6 +262,7 @@ class WEB_API Node
     bool children_are_inline() const { return has_flag(RustFFI::NodeFlag::ChildrenAreInline); }
     void set_children_are_inline(bool value) { set_flag(RustFFI::NodeFlag::ChildrenAreInline, value); }
 
+    bool is_editing_host() const { return has_flag(RustFFI::NodeFlag::IsEditingHost); }
     void set_is_editing_host(bool value) { set_flag(RustFFI::NodeFlag::IsEditingHost, value); }
 
     u32 initial_quote_nesting_level() const { return m_data->initial_quote_nesting_level; }
diff --git a/Libraries/LibWeb/Layout/TextNode.cpp b/Libraries/LibWeb/Layout/TextNode.cpp
index ebca33eba8e77..89660c433f73e 100644
--- a/Libraries/LibWeb/Layout/TextNode.cpp
+++ b/Libraries/LibWeb/Layout/TextNode.cpp
@@ -14,6 +14,8 @@
 #include <LibUnicode/CharacterTypes.h>
 #include <LibUnicode/Locale.h>
 #include <LibWeb/DOM/Document.h>
+#include <LibWeb/DOM/ShadowRoot.h>
+#include <LibWeb/HTML/FormAssociatedElement.h>
 #include <LibWeb/Layout/NodeArena.h>
 #include <LibWeb/Layout/TextNode.h>
 #include <LibWeb/Painting/InlinePaintable.h>
@@ -25,12 +27,14 @@ TextNode::TextNode(DOM::Document& document, DOM::Text& text)
     : Node(document, &text)
 {
     enroll_for_arena_text_content_sync();
+    update_produces_line_box_fragment_when_empty_flag();
 }
 
 TextNode::TextNode(DOM::Document& document, DOM::Text& text, AttachToDOMNode attach_to_dom_node)
     : Node(document, &text, attach_to_dom_node)
 {
     enroll_for_arena_text_content_sync();
+    update_produces_line_box_fragment_when_empty_flag();
 }
 
 TextNode::TextNode(DOM::Document& document)
@@ -39,6 +43,28 @@ TextNode::TextNode(DOM::Document& document)
     enroll_for_arena_text_content_sync();
 }
 
+bool TextNode::update_produces_line_box_fragment_when_empty_flag()
+{
+    // Text controls and editing hosts rely on their text node producing a zero-width fragment even
+    // when it has no text: the fragment keeps the line box alive with real font metrics, giving the
+    // caret an anchor to paint at and the control its baseline. Stamping this as a node flag keeps
+    // layout itself unaware of editing state.
+    auto produces_line_box_fragment_when_empty = [&] {
+        auto const* dom_text = this->dom_text();
+        if (!dom_text)
+            return false;
+        if (auto const* shadow_root = as_if<DOM::ShadowRoot>(dom_text->root())) {
+            if (as_if<HTML::FormAssociatedTextControlElement>(shadow_root->host()))
+                return true;
+        }
+        return dom_text->parent() && dom_text->parent()->is_editing_host();
+    }();
+    if (has_flag(RustFFI::NodeFlag::ProducesLineBoxFragmentWhenEmpty) == produces_line_box_fragment_when_empty)
+        return false;
+    set_flag(RustFFI::NodeFlag::ProducesLineBoxFragmentWhenEmpty, produces_line_box_fragment_when_empty);
+    return true;
+}
+
 TextNode::~TextNode() = default;
 
 DOM::Element const* TextNode::parent_element_for_text_transform() const
diff --git a/Libraries/LibWeb/Layout/TextNode.h b/Libraries/LibWeb/Layout/TextNode.h
index 84c3a88365633..fabe77528897e 100644
--- a/Libraries/LibWeb/Layout/TextNode.h
+++ b/Libraries/LibWeb/Layout/TextNode.h
@@ -48,6 +48,8 @@ class TextNode : public Node {
 
     void set_needs_repaint(InvalidateDisplayList = InvalidateDisplayList::Yes) const;
 
+    bool update_produces_line_box_fragment_when_empty_flag();
+
 protected:
     TextNode(DOM::Document&, DOM::Text&, AttachToDOMNode);
     explicit TextNode(DOM::Document&);
diff --git a/Libraries/LibWeb/Rust/src/layout/formatting_context.rs b/Libraries/LibWeb/Rust/src/layout/formatting_context.rs
index 55b3098a9729e..d87d0e7a0ea45 100644
--- a/Libraries/LibWeb/Rust/src/layout/formatting_context.rs
+++ b/Libraries/LibWeb/Rust/src/layout/formatting_context.rs
@@ -900,8 +900,6 @@ pub struct FfiLayoutFcCallbacks {
     pub release_anchor_name_handle: crate::layout::FfiReleaseAnchorNameHandleCallback,
     pub build_replaced_content_facts: unsafe extern "C" fn(*mut c_void, *mut c_void) -> crate::layout::FfiReplacedContentFacts,
     pub build_list_item_facts: unsafe extern "C" fn(*mut c_void, *mut c_void) -> crate::layout::FfiListItemFacts,
-    pub text_node_is_empty_editable: unsafe extern "C" fn(*mut c_void, *mut c_void) -> bool,
-    pub document_cursor_is_on_node: unsafe extern "C" fn(*mut c_void, *mut c_void) -> bool,
     pub build_svg_facts: unsafe extern "C" fn(*mut c_void, *mut c_void) -> FfiSvgElementFacts,
     pub read_paintable_geometry:
         unsafe extern "C" fn(*mut c_void, *mut c_void, *mut c_void, *mut crate::layout::FfiPaintableGeometry) -> bool,
diff --git a/Libraries/LibWeb/Rust/src/layout/inline_formatting_context.rs b/Libraries/LibWeb/Rust/src/layout/inline_formatting_context.rs
index ff6ff6405b276..be7d744a5e613 100644
--- a/Libraries/LibWeb/Rust/src/layout/inline_formatting_context.rs
+++ b/Libraries/LibWeb/Rust/src/layout/inline_formatting_context.rs
@@ -1225,11 +1225,6 @@ impl<'context, 'pass> InlineFormattingContext<'context, 'pass> {
 }
 
 impl LineBoxTextProvider for InlineFormattingContext<'_, '_> {
-    fn document_cursor_is_on_node(&self, node: Node) -> bool {
-        // SAFETY: The host reads document state synchronously.
-        unsafe { (self.callbacks.document_cursor_is_on_node)(self.callbacks.context, self.callbacks.shell(node)) }
-    }
-
     fn font_glyph_width(&self, font: *const c_void, code_point: u32) -> f32 {
         font_glyph_width(font, code_point)
     }
diff --git a/Libraries/LibWeb/Rust/src/layout/inline_level_iterator.rs b/Libraries/LibWeb/Rust/src/layout/inline_level_iterator.rs
index ac877c043e908..fc437d345c13c 100644
--- a/Libraries/LibWeb/Rust/src/layout/inline_level_iterator.rs
+++ b/Libraries/LibWeb/Rust/src/layout/inline_level_iterator.rs
@@ -397,18 +397,14 @@ impl<'iterator, 'context, 'pass> InlineLevelIteratorGenerator<'iterator, 'contex
             text_context.next_chunk_index += 1;
         }
         let mut is_last_chunk = text_context.next_chunk_index >= chunks.len();
-        let is_empty_editable = chunk.is_none()
+        let synthesize_zero_length_chunk = chunk.is_none()
             && is_first_chunk
             && is_last_chunk
             && text_context.text.is_empty()
-            && {
-                let callbacks = self.context().callbacks;
-                // SAFETY: The host reads the live TextNode synchronously.
-                unsafe { (callbacks.text_node_is_empty_editable)(callbacks.context, callbacks.shell(text_node)) }
-            };
+            && self.context().facts(text_node).produces_line_box_fragment_when_empty();
         let chunk = if let Some(chunk) = chunk {
             chunk
-        } else if is_empty_editable {
+        } else if synthesize_zero_length_chunk {
             text_context.next_chunk_index = 1;
             let parent_style = self.context().style(self.context().parent_node(text_node));
             TextChunk {
@@ -490,7 +486,7 @@ impl<'iterator, 'context, 'pass> InlineLevelIteratorGenerator<'iterator, 'contex
             style.letter_spacing().to_double() as f32,
         );
         let chunk_inline_size = CssPixels::nearest_value_for_f32(glyphs.width + inline_offset);
-        let generated_empty = is_empty_editable
+        let generated_empty = synthesize_zero_length_chunk
             || (self.context().facts(text_node).is_generated_for_pseudo_element() && chunk.length == 0);
         let mut item = Item::new(ItemType::Text, text_node);
         item.glyphs = Some(glyphs);
diff --git a/Libraries/LibWeb/Rust/src/layout/layout_state.rs b/Libraries/LibWeb/Rust/src/layout/layout_state.rs
index 9c2e3be56d67c..accadc65131c5 100644
--- a/Libraries/LibWeb/Rust/src/layout/layout_state.rs
+++ b/Libraries/LibWeb/Rust/src/layout/layout_state.rs
@@ -561,6 +561,10 @@ impl<'pass> NodeFacts<'pass> {
         crate::layout::has_flag(self.data(), NodeFlag::IsEditingHost)
     }
 
+    pub(crate) fn produces_line_box_fragment_when_empty(&self) -> bool {
+        crate::layout::has_flag(self.data(), NodeFlag::ProducesLineBoxFragmentWhenEmpty)
+    }
+
     pub(crate) fn uses_button_layout(&self) -> bool {
         crate::layout::has_flag(self.data(), NodeFlag::UsesButtonLayout)
     }
diff --git a/Libraries/LibWeb/Rust/src/layout/line_box.rs b/Libraries/LibWeb/Rust/src/layout/line_box.rs
index 81434c66e2341..d2400f5d79576 100644
--- a/Libraries/LibWeb/Rust/src/layout/line_box.rs
+++ b/Libraries/LibWeb/Rust/src/layout/line_box.rs
@@ -5,7 +5,6 @@
  */
 
 pub(crate) trait LineBoxTextProvider {
-    fn document_cursor_is_on_node(&self, node: Node) -> bool;
     fn font_glyph_width(&self, font: *const c_void, code_point: u32) -> f32;
 }
 
@@ -161,9 +160,6 @@ impl LineBoxData {
             }
             fragment_index -= 1;
             let fragment = &self.fragments[fragment_index];
-            if provider.document_cursor_is_on_node(fragment.layout_node) {
-                return whitespace_inline_size;
-            }
             if !matches!(
                 fragment.white_space_collapse,
                 white_space_collapse::COLLAPSE | white_space_collapse::PRESERVE_BREAKS
diff --git a/Libraries/LibWeb/Rust/src/layout/node_data.rs b/Libraries/LibWeb/Rust/src/layout/node_data.rs
index 02c8e67e3b0db..f116b8bdcf58c 100644
--- a/Libraries/LibWeb/Rust/src/layout/node_data.rs
+++ b/Libraries/LibWeb/Rust/src/layout/node_data.rs
@@ -141,6 +141,7 @@ pub enum NodeFlag {
     HasSavedAbsposLayoutInputs = 1 << 19,
     SavedAbsposCbDerivesFromOwnComputedValues = 1 << 20,
     SavedAbsposAlignmentDerivesFromOwnComputedValues = 1 << 21,
+    ProducesLineBoxFragmentWhenEmpty = 1 << 22,
 }
 
 #[repr(C)]
@@ -235,5 +236,6 @@ mod tests {
         assert_eq!(NodeFlag::UsesButtonLayout as u32, 1 << 16);
         assert_eq!(NodeFlag::IsEditingHost as u32, 1 << 17);
         assert_eq!(NodeFlag::ReplacedBoxCanHaveChildren as u32, 1 << 18);
+        assert_eq!(NodeFlag::ProducesLineBoxFragmentWhenEmpty as u32, 1 << 22);
     }
 }
diff --git a/Tests/LibWeb/Text/expected/Editing/caret-in-empty-text-node-after-contenteditable-toggle.txt b/Tests/LibWeb/Text/expected/Editing/caret-in-empty-text-node-after-contenteditable-toggle.txt
new file mode 100644
index 0000000000000..cd5fa711db430
--- /dev/null
+++ b/Tests/LibWeb/Text/expected/Editing/caret-in-empty-text-node-after-contenteditable-toggle.txt
@@ -0,0 +1,4 @@
+caret rect exists in freshly editable empty text node: true
+caret has line height: true
+empty editing host has line height while editable: true
+empty div collapses after contenteditable is removed: true
diff --git a/Tests/LibWeb/Text/expected/input-caret-advances-past-typed-trailing-space.txt b/Tests/LibWeb/Text/expected/input-caret-advances-past-typed-trailing-space.txt
new file mode 100644
index 0000000000000..aab3c86960c2f
--- /dev/null
+++ b/Tests/LibWeb/Text/expected/input-caret-advances-past-typed-trailing-space.txt
@@ -0,0 +1,3 @@
+input caret advances past first trailing space: true
+input caret advances past second trailing space: true
+editing host caret advances past trailing space: true
diff --git a/Tests/LibWeb/Text/input/Editing/caret-in-empty-text-node-after-contenteditable-toggle.html b/Tests/LibWeb/Text/input/Editing/caret-in-empty-text-node-after-contenteditable-toggle.html
new file mode 100644
index 0000000000000..063a1b593222f
--- /dev/null
+++ b/Tests/LibWeb/Text/input/Editing/caret-in-empty-text-node-after-contenteditable-toggle.html
@@ -0,0 +1,27 @@
+<!DOCTYPE html>
+<script src="../include.js"></script>
+<div></div>
+<script>
+test(() => {
+    // An empty text node produces a zero-width line box fragment only while its parent is an
+    // editing host, and that fact is stamped on the layout node. Toggling contenteditable at
+    // runtime must therefore refresh the stamp and relayout, or the caret would have no
+    // fragment to anchor to until some unrelated relayout runs.
+    const host = document.querySelector("div");
+    host.appendChild(document.createTextNode(""));
+    host.getBoundingClientRect();
+
+    host.setAttribute("contenteditable", "");
+    host.focus();
+    getSelection().collapse(host.firstChild, 0);
+    const caret_rect = internals.currentCaretRect();
+    println(`caret rect exists in freshly editable empty text node: ${caret_rect !== null}`);
+    println(`caret has line height: ${caret_rect !== null && caret_rect.height > 0}`);
+
+    const height_while_editable = host.getBoundingClientRect().height;
+    host.removeAttribute("contenteditable");
+    const height_after_removal = host.getBoundingClientRect().height;
+    println(`empty editing host has line height while editable: ${height_while_editable > 0}`);
+    println(`empty div collapses after contenteditable is removed: ${height_after_removal === 0}`);
+});
+</script>
diff --git a/Tests/LibWeb/Text/input/input-caret-advances-past-typed-trailing-space.html b/Tests/LibWeb/Text/input/input-caret-advances-past-typed-trailing-space.html
new file mode 100644
index 0000000000000..8971f69725574
--- /dev/null
+++ b/Tests/LibWeb/Text/input/input-caret-advances-past-typed-trailing-space.html
@@ -0,0 +1,30 @@
+<!DOCTYPE html>
+<script src="include.js"></script>
+<input>
+<div contenteditable></div>
+<script>
+test(() => {
+    // The caret must keep advancing while trailing spaces are typed, even though trailing
+    // whitespace at the end of a line would ordinarily be invisible: text control inner
+    // editors preserve all whitespace via white-space: pre, and typing into an editing host
+    // canonicalizes a would-collapse space into a non-breaking space.
+    const input_element = document.querySelector("input");
+    input_element.focus();
+    internals.sendText(input_element, "hi");
+    const input_caret_x_after_text = internals.currentCaretRect().x;
+    internals.sendText(input_element, " ");
+    const input_caret_x_after_first_trailing_space = internals.currentCaretRect().x;
+    internals.sendText(input_element, " ");
+    const input_caret_x_after_second_trailing_space = internals.currentCaretRect().x;
+    println(`input caret advances past first trailing space: ${input_caret_x_after_first_trailing_space > input_caret_x_after_text}`);
+    println(`input caret advances past second trailing space: ${input_caret_x_after_second_trailing_space > input_caret_x_after_first_trailing_space}`);
+
+    const editing_host = document.querySelector("div[contenteditable]");
+    editing_host.focus();
+    internals.sendText(editing_host, "hi");
+    const editing_host_caret_x_after_text = internals.currentCaretRect().x;
+    internals.sendText(editing_host, " ");
+    const editing_host_caret_x_after_trailing_space = internals.currentCaretRect().x;
+    println(`editing host caret advances past trailing space: ${editing_host_caret_x_after_trailing_space > editing_host_caret_x_after_text}`);
+});
+</script>