diff --git a/packages/eui/changelogs/upcoming/8950.md b/packages/eui/changelogs/upcoming/8950.md
new file mode 100644
index 00000000000..e68e639337b
--- /dev/null
+++ b/packages/eui/changelogs/upcoming/8950.md
@@ -0,0 +1,3 @@
+**Accessibility**
+
+- Fixed an issue where pressing Shift + Tab on the last tabbable element inside `EuiInputPopover` popover would close the popover unexpectedly
diff --git a/packages/eui/src/components/form/range/types.ts b/packages/eui/src/components/form/range/types.ts
index 09034cf1aee..0b25c471384 100644
--- a/packages/eui/src/components/form/range/types.ts
+++ b/packages/eui/src/components/form/range/types.ts
@@ -131,6 +131,7 @@ export interface _SharedRangeInputProps {
     | 'isOpen'
     | 'closePopover'
     | 'disableFocusTrap'
+    | 'ownFocus'
     | 'popoverScreenReaderText'
     | 'fullWidth'
   >;
diff --git a/packages/eui/src/components/popover/input_popover.spec.tsx b/packages/eui/src/components/popover/input_popover.spec.tsx
index 8a3b0a18938..d02d6373cc1 100644
--- a/packages/eui/src/components/popover/input_popover.spec.tsx
+++ b/packages/eui/src/components/popover/input_popover.spec.tsx
@@ -177,6 +177,22 @@ describe('EuiPopover', () => {
 
         cy.get('[data-popover-panel]').should('not.exist');
       });
+
+      it('does not close the popover when users Shift+Tab from the last item in the popover', () => {
+        cy.mount(
+          <StatefulInputPopover>
+            <button data-test-subj="one">one</button>
+            <button data-test-subj="two">two</button>
+          </StatefulInputPopover>
+        );
+
+        cy.focused().invoke('attr', 'data-test-subj').should('eq', 'one');
+        cy.realPress('Tab');
+        cy.focused().invoke('attr', 'data-test-subj').should('eq', 'two');
+        cy.realPress(['Shift', 'Tab']);
+        cy.focused().invoke('attr', 'data-test-subj').should('eq', 'one');
+        cy.get('[data-popover-panel]').should('exist');
+      });
     });
 
     describe('with focus trap disabled', () => {
@@ -192,24 +208,6 @@ describe('EuiPopover', () => {
         cy.get('[data-popover-panel]').should('exist');
       });
 
-      // Not sure how much sense this behavior makes, but this logic was
-      // apparently added to EuiInputPopover with EuiDualRange in mind
-      it('automatically closes the popover when users tab from anywhere in the popover', () => {
-        cy.mount(
-          <>
-            <StatefulInputPopover disableFocusTrap={true}>
-              <button data-test-subj="one">one</button>
-              <button data-test-subj="two">two</button>
-            </StatefulInputPopover>
-          </>
-        );
-
-        cy.get('[data-test-subj="one"]').click();
-        cy.realPress('Tab');
-
-        cy.get('[data-popover-panel]').should('not.exist');
-      });
-
       it('behaves with normal popover focus trap/tab behavior if `ownFocus` is set to true', () => {
         cy.mount(
           <>
diff --git a/packages/eui/src/components/popover/input_popover.stories.tsx b/packages/eui/src/components/popover/input_popover.stories.tsx
index eb7d4f8ecbf..3fcc72f38de 100644
--- a/packages/eui/src/components/popover/input_popover.stories.tsx
+++ b/packages/eui/src/components/popover/input_popover.stories.tsx
@@ -6,8 +6,9 @@
  * Side Public License, v 1.
  */
 
-import React, { useState } from 'react';
+import React, { MutableRefObject, useRef, useState } from 'react';
 import type { Meta, StoryObj } from '@storybook/react';
+import { css } from '@emotion/react';
 
 import {
   disableStorybookControls,
@@ -16,6 +17,7 @@ import {
 } from '../../../.storybook/utils';
 import { LOKI_SELECTORS } from '../../../.storybook/loki';
 import { EuiFieldText } from '../form';
+import { EuiButton } from '../button';
 import { EuiInputPopover, EuiInputPopoverProps } from './input_popover';
 
 const meta: Meta<EuiInputPopoverProps> = {
@@ -91,8 +93,16 @@ const StatefulInputPopover = ({
   isOpen: _isOpen,
   ...rest
 }: EuiInputPopoverProps) => {
+  const panelRef: MutableRefObject<HTMLElement | null> = useRef(null);
+
   const [isOpen, setOpen] = useState(_isOpen);
 
+  const setPanelRef = (node: HTMLElement | null) => {
+    setTimeout(() => {
+      panelRef.current = node;
+    });
+  };
+
   const handleOnClose = () => {
     setOpen(false);
     closePopover?.();
@@ -101,7 +111,15 @@ const StatefulInputPopover = ({
   const connectedInput = React.isValidElement(input)
     ? React.cloneElement(input, {
         ...input.props,
-        onFocus: () => setOpen(true),
+        onFocus: (e: React.FocusEvent) => {
+          if (
+            (e.relatedTarget != null &&
+              !panelRef.current?.contains(e.relatedTarget)) ||
+            (e.relatedTarget == null && !panelRef.current)
+          ) {
+            setOpen(true);
+          }
+        },
       })
     : input;
 
@@ -110,6 +128,7 @@ const StatefulInputPopover = ({
       isOpen={isOpen}
       closePopover={handleOnClose}
       input={connectedInput}
+      panelRef={setPanelRef}
       {...rest}
     >
       {children}
@@ -132,3 +151,37 @@ export const AnchorPosition: Story = {
     </div>
   ),
 };
+
+export const InteractiveChildren: Story = {
+  parameters: {
+    controls: { include: ['ownFocus', 'disableFocusTrap'] },
+    loki: {
+      skip: true,
+    },
+  },
+  args: {
+    input: (
+      <EuiFieldText
+        placeholder="Focus me to toggle an input popover"
+        aria-label="Popover attached to input element"
+      />
+    ),
+  },
+  render: (args) => (
+    <>
+      <StatefulInputPopover {...args}>
+        <div
+          css={({ euiTheme }) => css`
+            display: flex;
+            flex-direction: column;
+            gap: ${euiTheme.size.s};
+          `}
+        >
+          <EuiButton>First button</EuiButton>
+          <EuiButton>Second button</EuiButton>
+          <EuiButton>Third button</EuiButton>
+        </div>
+      </StatefulInputPopover>
+    </>
+  ),
+};
diff --git a/packages/eui/src/components/popover/input_popover.tsx b/packages/eui/src/components/popover/input_popover.tsx
index a852ec2a6a0..7eb6ddf2897 100644
--- a/packages/eui/src/components/popover/input_popover.tsx
+++ b/packages/eui/src/components/popover/input_popover.tsx
@@ -135,6 +135,28 @@ export const EuiInputPopover: FunctionComponent<EuiInputPopoverProps> = ({
 
   const panelPropsOnKeyDown = props.panelProps?.onKeyDown;
 
+  const handleTabNavigation = useCallback(
+    (e: KeyboardEvent<HTMLDivElement>) => {
+      const tabbableItems = tabbable(e.currentTarget).filter(
+        (el) => !el.hasAttribute('data-focus-guard')
+      );
+      if (!tabbableItems.length) return;
+
+      const tabbingFromFirstItemInPopover =
+        document.activeElement === tabbableItems[0];
+      const tabbingFromLastItemInPopover =
+        document.activeElement === tabbableItems[tabbableItems.length - 1];
+
+      if (
+        (tabbingFromFirstItemInPopover && e.shiftKey) ||
+        (tabbingFromLastItemInPopover && !e.shiftKey)
+      ) {
+        closePopover();
+      }
+    },
+    [closePopover]
+  );
+
   const onKeyDown = useCallback(
     (event: KeyboardEvent<HTMLDivElement>) => {
       panelPropsOnKeyDown?.(event);
@@ -142,24 +164,16 @@ export const EuiInputPopover: FunctionComponent<EuiInputPopoverProps> = ({
       if (event.key === keys.TAB) {
         if (disableFocusTrap) {
           if (!ownFocus) {
-            closePopover();
+            handleTabNavigation(event);
           }
         } else {
-          const tabbableItems = tabbable(event.currentTarget).filter(
-            (el) => !el.hasAttribute('data-focus-guard')
-          );
-          if (!tabbableItems.length) return;
-
-          const tabbingFromLastItemInPopover =
-            document.activeElement === tabbableItems[tabbableItems.length - 1];
-
-          if (tabbingFromLastItemInPopover) {
-            closePopover();
+          if (!ownFocus) {
+            handleTabNavigation(event);
           }
         }
       }
     },
-    [disableFocusTrap, ownFocus, closePopover, panelPropsOnKeyDown]
+    [disableFocusTrap, ownFocus, panelPropsOnKeyDown, handleTabNavigation]
   );
 
   /**