diff --git a/.changeset/breadcrumbs-measure-whole-crumb.md b/.changeset/breadcrumbs-measure-whole-crumb.md
new file mode 100644
index 00000000000..a51df97d18a
--- /dev/null
+++ b/.changeset/breadcrumbs-measure-whole-crumb.md
@@ -0,0 +1,5 @@
+---
+'@primer/react': patch
+---
+
+Breadcrumbs: Collapse crumbs that render more than one element (such as a link with a sibling button) when they no longer fit, instead of overflowing the container.
diff --git a/packages/react/src/Breadcrumbs/Breadcrumbs.tsx b/packages/react/src/Breadcrumbs/Breadcrumbs.tsx
index 05b26021a4b..7f04137af4c 100644
--- a/packages/react/src/Breadcrumbs/Breadcrumbs.tsx
+++ b/packages/react/src/Breadcrumbs/Breadcrumbs.tsx
@@ -101,6 +101,15 @@ function getContentWidth(nav: HTMLElement) {
   return nav.clientWidth - parseFloat(paddingLeft) - parseFloat(paddingRight)
 }
 
+// A crumb can render several nodes (e.g. a link and a sibling button, or text), so its width is
+// the extent of everything in the item except the separator.
+function getCrumbWidth(li: HTMLElement, range: Range) {
+  range.selectNodeContents(li)
+  const last = li.lastElementChild
+  if (last?.classList.contains(classes.ItemSeparator)) range.setEndBefore(last)
+  return range.getBoundingClientRect().width
+}
+
 const sameFit = (a: Fit, b: Fit) => a.extra === b.extra && a.rootCollapsed === b.rootCollapsed && a.narrow === b.narrow
 
 // eslint-disable-next-line @typescript-eslint/no-explicit-any
@@ -213,15 +222,15 @@ function Breadcrumbs({className, children, style, overflow = 'wrap', variant = '
       const previous = widthsRef.current
       const widths = new Map<React.Key, number>()
       let separators = separatorsRef.current
+      const range = nav.ownerDocument.createRange()
       for (const item of items) {
         const width = previous.get(item.key ?? '')
         if (width !== undefined) widths.set(item.key ?? '', width)
       }
       for (const li of nav.querySelectorAll<HTMLElement>(':scope > ol > li[data-index]')) {
         const key = items[Number(li.getAttribute('data-index'))]?.key
-        const crumb = li.firstElementChild
-        if (key == null || !crumb) continue
-        const crumbWidth = crumb.getBoundingClientRect().width
+        if (key == null) continue
+        const crumbWidth = getCrumbWidth(li, range)
         widths.set(key, crumbWidth)
         if (li.nextElementSibling && !li.hasAttribute('data-collapsed')) {
           const separator = li.getBoundingClientRect().width - crumbWidth
diff --git a/packages/react/src/Breadcrumbs/__tests__/BreadcrumbsOverflow.test.tsx b/packages/react/src/Breadcrumbs/__tests__/BreadcrumbsOverflow.test.tsx
index a5e1c49e229..a8abd563646 100644
--- a/packages/react/src/Breadcrumbs/__tests__/BreadcrumbsOverflow.test.tsx
+++ b/packages/react/src/Breadcrumbs/__tests__/BreadcrumbsOverflow.test.tsx
@@ -395,6 +395,52 @@ describe('Breadcrumbs overflow regressions (real layout)', () => {
     expect(linksWithinNav()).toBe(true)
   })
 
+  it('measures every element a crumb renders, so it collapses instead of spilling out', async () => {
+    // Mirrors a header crumb that renders a link and a sibling button (a repository picker) in a
+    // region that aligns to the end, so an under-measured crumb would spill out of its start edge.
+    function CrumbWithPicker() {
+      return (
+        <>
+          <Breadcrumbs.Item href="#repository" selected>
+            repository
+          </Breadcrumbs.Item>
+          <button type="button" style={{width: 24}}>
+            Switch
+          </button>
+        </>
+      )
+    }
+    const ui = (width: number) => (
+      <div data-testid="region" style={{display: 'flex', justifyContent: 'flex-end', width}}>
+        <Breadcrumbs overflow="menu">
+          <Breadcrumbs.Item key="owner" href="#owner">
+            organization-with-a-long-name
+          </Breadcrumbs.Item>
+          <CrumbWithPicker key="repository" />
+        </Breadcrumbs>
+      </div>
+    )
+    const {rerender} = render(ui(800))
+    await nextFrame()
+    expect(menuButton()).toBeNull()
+
+    // Narrower than the crumbs, but wider than they measure without the picker button.
+    rerender(ui(screen.getByRole('list').getBoundingClientRect().width - 8))
+    await nextFrame()
+    expect(visibleLinks()).toEqual(['repository'])
+    const region = screen.getByTestId('region').getBoundingClientRect()
+    for (const element of [
+      menuButton()!,
+      ...screen.getAllByRole('link'),
+      screen.getByRole('button', {name: 'Switch'}),
+    ]) {
+      const rect = element.getBoundingClientRect()
+      if (rect.width === 0) continue
+      expect(rect.left).toBeGreaterThanOrEqual(region.left - 1)
+      expect(rect.right).toBeLessThanOrEqual(region.right + 1)
+    }
+  })
+
   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>