diff --git a/.changeset/breadcrumbs-shrink-in-flex-row.md b/.changeset/breadcrumbs-shrink-in-flex-row.md
new file mode 100644
index 00000000000..74d6ef66ad6
--- /dev/null
+++ b/.changeset/breadcrumbs-shrink-in-flex-row.md
@@ -0,0 +1,5 @@
+---
+'@primer/react': patch
+---
+
+Breadcrumbs: In `menu` and `menu-with-root` overflow modes, collapse crumbs as soon as they no longer fit beside sibling content in a flex row, so the collapse point no longer depends on crumb length or resize direction.
diff --git a/packages/react/src/Breadcrumbs/Breadcrumbs.module.css b/packages/react/src/Breadcrumbs/Breadcrumbs.module.css
index 7f0a0e49277..2e52b9091d6 100644
--- a/packages/react/src/Breadcrumbs/Breadcrumbs.module.css
+++ b/packages/react/src/Breadcrumbs/Breadcrumbs.module.css
@@ -10,6 +10,13 @@
   margin-bottom: 0;
 }
 
+/* The menu modes fit the crumbs to the width the parent offers. As a flex item the nav would
+   otherwise never shrink below its crumbs, so they would always measure as fitting and nothing
+   would collapse until the parent was narrower than every crumb together. */
+.BreadcrumbsBase:where([data-overflow^='menu']) {
+  min-width: 0;
+}
+
 [data-overflow='menu'],
 [data-overflow='menu-with-root'] {
   & .BreadcrumbsList {
diff --git a/packages/react/src/Breadcrumbs/__tests__/BreadcrumbsOverflow.test.tsx b/packages/react/src/Breadcrumbs/__tests__/BreadcrumbsOverflow.test.tsx
index a8abd563646..2bea4fbc9d8 100644
--- a/packages/react/src/Breadcrumbs/__tests__/BreadcrumbsOverflow.test.tsx
+++ b/packages/react/src/Breadcrumbs/__tests__/BreadcrumbsOverflow.test.tsx
@@ -441,6 +441,33 @@ describe('Breadcrumbs overflow regressions (real layout)', () => {
     }
   })
 
+  it('collapses when it shares a flex row with a sibling that can shrink', async () => {
+    // Mirrors a header region where the crumbs sit beside a search field. If the nav kept its
+    // crumbs' width, the sibling would absorb the squeeze and the crumbs would always measure as
+    // fitting, so nothing would collapse until the row was narrower than the crumbs alone.
+    // Whole-pixel widths, so rounding can't decide whether the crumbs fit.
+    const ui = (width: number) => (
+      <div style={{display: 'flex', width, ['--text-body-size-medium' as string]: '20px'}}>
+        <Breadcrumbs overflow="menu">
+          {['owner', 'repository'].map((label, index) => (
+            <Breadcrumbs.Item key={label} href={`#${label}`} selected={index === 1} style={{width: 150}}>
+              {label}
+            </Breadcrumbs.Item>
+          ))}
+        </Breadcrumbs>
+        <div style={{flex: '0 1 400px', minWidth: 100}} />
+      </div>
+    )
+    const {rerender} = render(ui(1600))
+    await nextFrame()
+    expect(menuButton()).toBeNull()
+
+    // The crumbs only fit if the sibling gives up everything above its minimum width.
+    rerender(ui(screen.getByRole('list').getBoundingClientRect().width + 100))
+    await nextFrame()
+    expect(visibleLinks()).toEqual(['repository'])
+  })
+
   it('starts with the overflow menu closed after switching to wrap and back', async () => {
     const user = userEvent.setup()
     const ui = (overflow: 'wrap' | 'menu') => <div style={{width: 300}}>{crumbs(overflow, labels)}</div>