diff --git a/packages/trees/src/components/OverflowText.tsx b/packages/trees/src/components/OverflowText.tsx
index a382278c6..c46f2e331 100644
--- a/packages/trees/src/components/OverflowText.tsx
+++ b/packages/trees/src/components/OverflowText.tsx
@@ -20,9 +20,17 @@ export interface OverflowTextProps extends PropsWithChildren {
   className?: string;
   marker?: ComponentChildren | ((props: MarkerProps) => ComponentChildren);
   variant?: 'default' | 'fade';
+  // Stands in for `children` in the hidden copy that detects overflow. Only the
+  // text metrics of that copy matter, so pass a plain-text equivalent when
+  // `children` holds things that should exist once in the DOM: data attributes
+  // that get queried, ids, form controls.
+  measureChildren?: ComponentChildren;
 }
 
-export type MiddleTruncateProps = Omit<OverflowTextProps, 'mode' | 'children'> &
+export type MiddleTruncateProps = Omit<
+  OverflowTextProps,
+  'mode' | 'children' | 'measureChildren'
+> &
   AllowableContentGroups & {
     minimumLength?: number;
     priority?: 'start' | 'end' | 'equal';
@@ -51,10 +59,14 @@ type AllowableContentGroups =
   | {
       children?: never;
       contents: [ComponentChildren, ComponentChildren];
+      // Per-segment stand-ins for the hidden copies that detect overflow, in the
+      // same order as `contents`. See `measureChildren` on OverflowTextProps.
+      measureContents?: [ComponentChildren, ComponentChildren];
     }
   | {
       contents?: never;
       children: string;
+      measureContents?: never;
     };
 
 // When a split boundary lands adjacent to whitespace, the trailing/leading
@@ -210,7 +222,8 @@ function OverflowMarker({
 
 function OverflowContent(options: OverflowTextProps) {
   'use no memo';
-  const { mode, children } = options;
+  const { mode, children, measureChildren } = options;
+  const overflowChildren = measureChildren ?? children;
 
   // The inner span wrapper here is only needed to implement
   // the right aligned internals for fruncate
@@ -220,7 +233,11 @@ function OverflowContent(options: OverflowTextProps) {
         {mode === 'fruncate' ? <span>{children}</span> : children}
       </div>
       <div data-truncate-content="overflow" aria-hidden>
-        {mode === 'fruncate' ? <span>{children}</span> : children}
+        {mode === 'fruncate' ? (
+          <span>{overflowChildren}</span>
+        ) : (
+          overflowChildren
+        )}
       </div>
     </div>
   );
@@ -228,6 +245,7 @@ function OverflowContent(options: OverflowTextProps) {
 
 export function OverflowText({
   children,
+  measureChildren,
   mode = 'truncate',
   marker = '…',
   variant = 'default',
@@ -235,7 +253,11 @@ export function OverflowText({
 }: OverflowTextProps): JSX.Element {
   'use no memo';
   const contentNode = (
-    <OverflowContent key="content" mode={mode}>
+    <OverflowContent
+      key="content"
+      mode={mode}
+      measureChildren={measureChildren}
+    >
       {children}
     </OverflowContent>
   );
@@ -291,6 +313,7 @@ export function Fruncate({
 export function MiddleTruncate({
   children,
   contents,
+  measureContents,
   priority = 'end',
   split = 'center',
   minimumLength = 12,
@@ -306,8 +329,16 @@ export function MiddleTruncate({
       console.error('MiddleTruncate: contents must be an array of two items');
       return null;
     }
-    firstSegment = <Truncate {...props}>{contents[0]}</Truncate>;
-    secondSegment = <Fruncate {...props}>{contents[1]}</Fruncate>;
+    firstSegment = (
+      <Truncate {...props} measureChildren={measureContents?.[0]}>
+        {contents[0]}
+      </Truncate>
+    );
+    secondSegment = (
+      <Fruncate {...props} measureChildren={measureContents?.[1]}>
+        {contents[1]}
+      </Fruncate>
+    );
   } else {
     // TODO: figure out how to support ReactNode children in the future
     if (typeof children !== 'string') {
diff --git a/packages/trees/src/render/FileTreeView.tsx b/packages/trees/src/render/FileTreeView.tsx
index de219c62b..38eb1d73e 100644
--- a/packages/trees/src/render/FileTreeView.tsx
+++ b/packages/trees/src/render/FileTreeView.tsx
@@ -1,6 +1,6 @@
 /** @jsxImportSource preact */
 import { Fragment } from 'preact';
-import type { JSX } from 'preact';
+import type { ComponentChildren, JSX } from 'preact';
 import {
   useCallback,
   useEffect,
@@ -41,6 +41,7 @@ import type {
   FileTreeItemHandle,
   FileTreeRowDecoration,
   FileTreeVisibleRow,
+  FileTreeVisibleSegment,
 } from '../model/publicTypes';
 import {
   FILE_TREE_DEFAULT_ITEM_HEIGHT,
@@ -86,30 +87,86 @@ function formatFlattenedSegments(
     return renameInput ?? row.name;
   }
 
-  return (
-    <span data-item-flattened-subitems>
-      {segments.map((segment, index) => {
-        const isLast = index === segments.length - 1;
-        return (
+  const isRenaming = renameInput != null;
+
+  const renderSegment = (
+    segment: FileTreeVisibleSegment,
+    content: ComponentChildren
+  ): JSX.Element => (
+    <span
+      key={segment.path}
+      data-item-flattened-subitem={segment.path}
+      data-item-flattened-subitem-drag-target={
+        dragTargetFlattenedSegmentPath === segment.path ? 'true' : undefined
+      }
+    >
+      {content}
+    </span>
+  );
+
+  // Renaming keeps every segment on a flex line of its own, where the terminal
+  // segment becomes the input. The input sizes itself against a flex item, and
+  // it has to stay visible rather than be truncated away.
+  if (isRenaming) {
+    return (
+      <span data-item-flattened-subitems>
+        {segments.map((segment, index) => (
           <Fragment key={segment.path}>
-            <span
-              data-item-flattened-subitem={segment.path}
-              data-item-flattened-subitem-drag-target={
-                dragTargetFlattenedSegmentPath === segment.path
-                  ? 'true'
-                  : undefined
-              }
-            >
-              {isLast && renameInput != null ? (
+            {renderSegment(
+              segment,
+              index === segments.length - 1 ? (
                 renameInput
               ) : (
                 <Truncate>{segment.name}</Truncate>
-              )}
-            </span>
+              )
+            )}
             {index < segments.length - 1 ? ' / ' : ''}
           </Fragment>
-        );
-      })}
+        ))}
+      </span>
+    );
+  }
+
+  // Otherwise the path splits at its last separator, the same place the
+  // `leaf-path` split picks. Truncating each segment on its own spent the row on
+  // ellipses ("t… / kc… / … / se…") instead of on the path; truncating the run
+  // as a whole would drop the terminal directory, which is the one the row
+  // actually opens. So the leading run absorbs the shrinking and the terminal
+  // directory holds its ground: "test / kotlin / com… / server".
+  const leading = segments.slice(0, -1);
+  const terminal = segments[segments.length - 1];
+  if (terminal == null) {
+    return row.name;
+  }
+
+  // This separator opens the terminal segment, so its leading space lands at
+  // the start of that line box, where the browser collapses it away ("b/ c").
+  // A non-breaking space survives.
+  const terminalSeparator = '\u00a0/ ';
+
+  // The hidden copies that detect overflow measure the same text without
+  // duplicating the per-segment markup that drag and drop and the tests query.
+  const leadingText = leading.map((segment) => segment.name).join(' / ');
+  const terminalText = `${terminalSeparator}${terminal.name}`;
+
+  return (
+    <span data-item-flattened-subitems>
+      <MiddleTruncate
+        priority="end"
+        contents={[
+          leading.map((segment, index) => (
+            <Fragment key={segment.path}>
+              {renderSegment(segment, segment.name)}
+              {index < leading.length - 1 ? ' / ' : ''}
+            </Fragment>
+          )),
+          <Fragment key={terminal.path}>
+            {terminalSeparator}
+            {renderSegment(terminal, terminal.name)}
+          </Fragment>,
+        ]}
+        measureContents={[leadingText, terminalText]}
+      />
     </span>
   );
 }
diff --git a/packages/trees/src/style.css b/packages/trees/src/style.css
index ef8e2d267..8661f6f9f 100644
--- a/packages/trees/src/style.css
+++ b/packages/trees/src/style.css
@@ -856,8 +856,10 @@
       z-index: 2;
 
       /* Flattened segment markers sit high enough to cover the row outline unless
-       * their painted background is inset by the focus ring width. */
-      [data-item-flattened-subitems] {
+       * their painted background is inset by the focus ring width. The marker
+       * sits outside the segments themselves, so inset from the section that
+       * contains them. */
+      [data-item-section='content']:has([data-item-flattened-subitems]) {
         --truncate-marker-block-inset: var(--trees-focus-ring-width);
       }
 
@@ -930,7 +932,21 @@
   }
 
   /* Flattened Directory Parts */
+  /*
+  Outside renaming the segments are a middle-truncate group, so the leading run
+  can shrink while the terminal directory holds its width. As flex items each
+  segment shrank and truncated on its own, which spent a narrow row on ellipses
+  rather than on the path.
+  */
   [data-item-flattened-subitems] {
+    display: block;
+    min-width: 0;
+  }
+  /*
+  Renaming swaps the terminal segment for an input, which sizes itself against a
+  flex item rather than against the row.
+  */
+  [data-item-flattened-subitems]:has([data-item-rename-input]) {
     display: inline-flex;
     align-items: center;
     gap: 2px;
diff --git a/packages/trees/test/e2e/file-tree-composition.pw.ts b/packages/trees/test/e2e/file-tree-composition.pw.ts
index ae898aeda..33a724be4 100644
--- a/packages/trees/test/e2e/file-tree-composition.pw.ts
+++ b/packages/trees/test/e2e/file-tree-composition.pw.ts
@@ -341,6 +341,70 @@ test.describe('file-tree composition surfaces', () => {
     expect(fileMarkerPadding.bottom).toBe(0);
   });
 
+  test('a narrow flattened row truncates the leading run and keeps the terminal directory', async ({
+    page,
+  }) => {
+    await page.goto('/test/e2e/fixtures/file-tree-composition.html');
+    await page.waitForFunction(
+      () => window.__fileTreeCompositionFixtureReady === true
+    );
+
+    const measureFlattenedRow = (mountWidth: string) =>
+      page.evaluate((width) => {
+        const mount = document.querySelector(
+          '[data-file-tree-composition-mount]'
+        );
+        if (!(mount instanceof HTMLElement)) {
+          throw new Error('Expected file-tree composition mount.');
+        }
+        mount.style.width = width;
+
+        const host = document.querySelector('file-tree-container');
+        const row = Array.from(
+          host?.shadowRoot?.querySelectorAll('button[data-type="item"]') ?? []
+        ).find(
+          (candidate) =>
+            candidate.querySelector('[data-item-flattened-subitems]') != null
+        );
+        if (!(row instanceof HTMLElement)) {
+          throw new Error(
+            'Expected a flattened row in the composition fixture.'
+          );
+        }
+
+        const segments = Array.from(
+          row.querySelectorAll('[data-item-flattened-subitem]')
+        );
+        const terminal = segments.at(-1);
+
+        return {
+          // A segment carrying its own marker is a segment truncating alone.
+          segmentsWithOwnMarker: segments.filter(
+            (segment) => segment.querySelector('[data-truncate-marker]') != null
+          ).length,
+          segmentCount: segments.length,
+          terminalName: terminal?.textContent ?? null,
+          terminalWidth: terminal?.getBoundingClientRect().width ?? 0,
+        };
+      }, mountWidth);
+
+    const wide = await measureFlattenedRow('360px');
+    expect(wide.segmentCount).toBeGreaterThan(1);
+
+    const narrow = await measureFlattenedRow('120px');
+
+    // Narrowing the row spends the shrinking on the leading run. Every segment
+    // truncating on its own is what left a deep path rendering as
+    // "t… / kc… / … / se…", with none of it readable.
+    expect(wide.segmentsWithOwnMarker).toBe(0);
+    expect(narrow.segmentsWithOwnMarker).toBe(0);
+
+    // The terminal directory is the one the row opens, so it keeps its width
+    // rather than being truncated away with the rest of the path.
+    expect(narrow.terminalName).toBe(wide.terminalName);
+    expect(narrow.terminalWidth).toBeCloseTo(wide.terminalWidth, 1);
+  });
+
   test('keyboard navigation retargets the focused row trigger away from a stale hover', async ({
     page,
   }) => {
diff --git a/packages/trees/test/file-tree-keyboard-selection.test.ts b/packages/trees/test/file-tree-keyboard-selection.test.ts
index aed3c32af..241a777de 100644
--- a/packages/trees/test/file-tree-keyboard-selection.test.ts
+++ b/packages/trees/test/file-tree-keyboard-selection.test.ts
@@ -499,17 +499,35 @@ describe('file-tree keyboard and selection', () => {
         '[data-item-flattened-subitems]'
       );
 
-      expect(flattenedContainer?.innerHTML).toContain(' / ');
-      expect(
+      // The rendered path reads as one run. The separator opening the terminal
+      // segment uses a non-breaking space so it survives at the start of its
+      // line box.
+      const visibleText = Array.from(
         flattenedContainer?.querySelectorAll(
-          ':scope > [data-item-flattened-subitem]'
-        ).length
-      ).toBe(2);
+          '[data-truncate-content="visible"]'
+        ) ?? []
+      )
+        .map((node) => node.textContent)
+        .join('');
+      expect(visibleText).toBe('src\u00a0/ lib');
+
+      // Each segment is in the DOM once. The copies that measure overflow carry
+      // plain text, so they never duplicate a segment's identity.
+      expect(
+        Array.from(
+          flattenedContainer?.querySelectorAll(
+            '[data-item-flattened-subitem]'
+          ) ?? []
+        ).map((node) => node.getAttribute('data-item-flattened-subitem'))
+      ).toEqual(['src/', 'src/lib/']);
+
+      // No span exists solely to hold a separator, which would make it a hover
+      // and drop target of its own.
       expect(
-        flattenedContainer?.querySelector(
-          ':scope > span:not([data-item-flattened-subitem])'
+        Array.from(flattenedContainer?.querySelectorAll('span') ?? []).some(
+          (node) => node.textContent?.trim() === '/'
         )
-      ).toBeNull();
+      ).toBe(false);
 
       fileTree.cleanUp();
     } finally {