diff --git a/changelogs/upcoming/7555.md b/changelogs/upcoming/7555.md
new file mode 100644
index 00000000000..b827da815c6
--- /dev/null
+++ b/changelogs/upcoming/7555.md
@@ -0,0 +1 @@
+- `EuiBreadcrumbs`'s `popoverContent` API now accepts a render function that will be passed a `closePopover` callback, allowing consumers to close the breadcrumb popover from their popover content
diff --git a/src-docs/src/views/breadcrumbs/breadcrumbs_example.js b/src-docs/src/views/breadcrumbs/breadcrumbs_example.js
index 9d3ec472d66..53fe2dd0d9e 100644
--- a/src-docs/src/views/breadcrumbs/breadcrumbs_example.js
+++ b/src-docs/src/views/breadcrumbs/breadcrumbs_example.js
@@ -294,6 +294,14 @@ export const BreadcrumbsExample = {
             accepted as they are controlled automatically by{' '}
             <strong>EuiBreadcrumbs</strong>.
           </p>
+          <p>
+            If you need the ability to close the breadcrumb popover from within
+            your popover content, <EuiCode>popoverContent</EuiCode> accepts a
+            render function that will be passed a{' '}
+            <EuiCode>closePopover</EuiCode> callback, which you can invoke to
+            close the popover. See the Deployment breadcrumb below for example
+            usage.
+          </p>
           <EuiCallOut
             color="warning"
             iconType="accessibility"
diff --git a/src-docs/src/views/breadcrumbs/popover_content.tsx b/src-docs/src/views/breadcrumbs/popover_content.tsx
index f5ab29a0198..9088af0b38f 100644
--- a/src-docs/src/views/breadcrumbs/popover_content.tsx
+++ b/src-docs/src/views/breadcrumbs/popover_content.tsx
@@ -41,37 +41,34 @@ export default () => {
   const breadcrumbs: EuiBreadcrumb[] = [
     {
       text: 'My deployment',
-      popoverContent: (
-        <>
-          <EuiPopoverTitle paddingSize="s">Select a deployment</EuiPopoverTitle>
-          <EuiContextMenuPanel
-            size="s"
-            items={[
-              <EuiContextMenuItem
-                key="A"
-                href="#"
-                onClick={(e) => e.preventDefault()}
-              >
-                Go to Deployment A
-              </EuiContextMenuItem>,
-              <EuiContextMenuItem
-                key="B"
-                href="#"
-                onClick={(e) => e.preventDefault()}
-              >
-                Go to Deployment B
-              </EuiContextMenuItem>,
-              <EuiContextMenuItem
-                key="C"
-                href="#"
-                onClick={(e) => e.preventDefault()}
-              >
-                Go to all deployments
-              </EuiContextMenuItem>,
-            ]}
-          />
-        </>
-      ),
+      // Passing a render function allows closing the breadcrumb popover from within your content
+      popoverContent: (closePopover) => {
+        const onClick = (e: React.MouseEvent) => {
+          e.preventDefault();
+          closePopover();
+        };
+        return (
+          <>
+            <EuiPopoverTitle paddingSize="s">
+              Select a deployment
+            </EuiPopoverTitle>
+            <EuiContextMenuPanel
+              size="s"
+              items={[
+                <EuiContextMenuItem key="A" href="#" onClick={onClick}>
+                  Go to Deployment A
+                </EuiContextMenuItem>,
+                <EuiContextMenuItem key="B" href="#" onClick={onClick}>
+                  Go to Deployment B
+                </EuiContextMenuItem>,
+                <EuiContextMenuItem key="C" href="#" onClick={onClick}>
+                  Go to all deployments
+                </EuiContextMenuItem>,
+              ]}
+            />
+          </>
+        );
+      },
       popoverProps: { panelPaddingSize: 'none' },
     },
     {
diff --git a/src/components/breadcrumbs/__snapshots__/breadcrumb.test.tsx.snap b/src/components/breadcrumbs/__snapshots__/breadcrumb.test.tsx.snap
index 5a803bb40ce..116e054b27e 100644
--- a/src/components/breadcrumbs/__snapshots__/breadcrumb.test.tsx.snap
+++ b/src/components/breadcrumbs/__snapshots__/breadcrumb.test.tsx.snap
@@ -1,6 +1,6 @@
 // Jest Snapshot v1, https://goo.gl/fbAQLP
 
-exports[`EuiBreadcrumbContent renders breadcrumbs with \`popoverContent\` with popovers 1`] = `
+exports[`EuiBreadcrumbContent breadcrumbs with popovers renders with \`popoverContent\` 1`] = `
 <body>
   <div>
     <div
diff --git a/src/components/breadcrumbs/breadcrumb.test.tsx b/src/components/breadcrumbs/breadcrumb.test.tsx
index a5e2d4607fe..e15addfa4f4 100644
--- a/src/components/breadcrumbs/breadcrumb.test.tsx
+++ b/src/components/breadcrumbs/breadcrumb.test.tsx
@@ -8,7 +8,11 @@
 
 import React from 'react';
 import { fireEvent } from '@testing-library/react';
-import { render, waitForEuiPopoverOpen } from '../../test/rtl';
+import {
+  render,
+  waitForEuiPopoverOpen,
+  waitForEuiPopoverClose,
+} from '../../test/rtl';
 
 import { EuiBreadcrumbContent } from './breadcrumb';
 
@@ -35,21 +39,44 @@ describe('EuiBreadcrumbContent', () => {
     expect(container).toMatchSnapshot();
   });
 
-  it('renders breadcrumbs with `popoverContent` with popovers', async () => {
-    const { baseElement, getByTestSubject } = render(
-      <EuiBreadcrumbContent
-        type="page"
-        text="Toggles a popover"
-        data-test-subj="popoverToggle"
-        popoverContent="Hello popover world"
-        popoverProps={{ 'data-test-subj': 'popover' }}
-      />
-    );
-    fireEvent.click(getByTestSubject('popoverToggle'));
-    await waitForEuiPopoverOpen();
+  describe('breadcrumbs with popovers', () => {
+    it('renders with `popoverContent`', async () => {
+      const { baseElement, getByTestSubject } = render(
+        <EuiBreadcrumbContent
+          type="page"
+          text="Toggles a popover"
+          data-test-subj="popoverToggle"
+          popoverContent="Hello popover world"
+          popoverProps={{ 'data-test-subj': 'popover' }}
+        />
+      );
+      fireEvent.click(getByTestSubject('popoverToggle'));
+      await waitForEuiPopoverOpen();
 
-    expect(getByTestSubject('popover')).toBeInTheDocument();
-    expect(baseElement).toMatchSnapshot();
+      expect(getByTestSubject('popover')).toBeInTheDocument();
+      expect(baseElement).toMatchSnapshot();
+    });
+
+    it('passes a popover close callback to `popoverContent` render functions', async () => {
+      const { getByTestSubject } = render(
+        <EuiBreadcrumbContent
+          type="page"
+          text="Controlled breadcrumb popover"
+          data-test-subj="popoverToggle"
+          popoverContent={(closePopover) => (
+            <button onClick={closePopover} data-test-subj="popoverClose">
+              Close popover
+            </button>
+          )}
+        />
+      );
+
+      fireEvent.click(getByTestSubject('popoverToggle'));
+      await waitForEuiPopoverOpen();
+
+      fireEvent.click(getByTestSubject('popoverClose'));
+      await waitForEuiPopoverClose();
+    });
   });
 
   describe('highlightLastBreadcrumb', () => {
diff --git a/src/components/breadcrumbs/breadcrumb.tsx b/src/components/breadcrumbs/breadcrumb.tsx
index 5730e219dc3..13daeef593e 100644
--- a/src/components/breadcrumbs/breadcrumb.tsx
+++ b/src/components/breadcrumbs/breadcrumb.tsx
@@ -56,12 +56,14 @@ export type EuiBreadcrumbProps = Omit<
      */
     'aria-current'?: AriaAttributes['aria-current'];
     /**
-     * Creates a breadcrumb that toggles a popover dialog
+     * Creates a breadcrumb that toggles a popover dialog. Takes any rendered node(s),
+     * or a render function that will pass callback allowing you to close the
+     * breadcrumb popover from within your popover content.
      *
      * If passed, both `href` and `onClick` will be ignored - the breadcrumb's
      * click behavior should only trigger a popover.
      */
-    popoverContent?: ReactNode;
+    popoverContent?: ReactNode | ((closePopover: () => void) => ReactNode);
     /**
      * Allows customizing the popover if necessary. Accepts any props that
      * [EuiPopover](/#/layout/popover) accepts, except for props that control state.
@@ -166,11 +168,12 @@ export const EuiBreadcrumbContent: FunctionComponent<
         const styleProps = { className: classes, css: cssStyles };
 
         if (isPopoverBreadcrumb) {
+          const closePopover = () => setIsPopoverOpen(false);
           return (
             <EuiPopover
               {...popoverProps}
               isOpen={isPopoverOpen}
-              closePopover={() => setIsPopoverOpen(false)}
+              closePopover={closePopover}
               css={!isLastBreadcrumb && styles.euiBreadcrumb__popoverWrapper}
               button={
                 <EuiLink
@@ -190,7 +193,9 @@ export const EuiBreadcrumbContent: FunctionComponent<
                 </EuiLink>
               }
             >
-              {popoverContent}
+              {typeof popoverContent === 'function'
+                ? popoverContent(closePopover)
+                : popoverContent}
             </EuiPopover>
           );
         } else if (isInteractiveBreadcrumb) {