diff --git a/CHANGELOG.md b/CHANGELOG.md
index dfde4e6b1bf..e6123b92ddf 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -14,6 +14,8 @@ No public interface changes since `37.7.0`.
 - Refactored styles of `EuiTabs` ([#5135](https://github.com/elastic/eui/pull/5135))
 - Removed Sass variables for `EuiTabs` font size (`$euiTabFontSize, $euiTabFontSizeS, $euiTabFontSizeL`) ([#5135](https://github.com/elastic/eui/pull/5135))
 - Extended all `EuiTabProps` for each `EuiTabbedContentTab` ([#5135](https://github.com/elastic/eui/pull/5135))
+- Changed `EuiPopover`'s `repositionOnScroll` function to prevent popover and input elements from separating on scroll when nested in `EuiFlyout` ([#5155](https://github.com/elastic/eui/pull/5155))
+- Added the `repositionOnScroll` prop to `EuiSuperSelect` ([#5155](https://github.com/elastic/eui/pull/5155)) 
 - Added `useGeneratedHtmlId` utility, which memoizes the randomly generated ID on mount and prevents regenerated IDs on component rerender ([#5133](https://github.com/elastic/eui/pull/5133))
 - Fixed `z-index` styles that were causing parts of `EuiResizableContainer` to overlap `EuiHeader` ([#5164](https://github.com/elastic/eui/pull/5164))
 
diff --git a/src-docs/src/views/flyout/flyout_complicated.js b/src-docs/src/views/flyout/flyout_complicated.js
index ac0a0f09553..de76084edb5 100644
--- a/src-docs/src/views/flyout/flyout_complicated.js
+++ b/src-docs/src/views/flyout/flyout_complicated.js
@@ -3,6 +3,7 @@ import React, { useState, Fragment } from 'react';
 import {
   EuiButton,
   EuiButtonEmpty,
+  EuiCode,
   EuiCodeBlock,
   EuiComboBox,
   EuiExpression,
@@ -207,11 +208,16 @@ export default () => {
               </EuiButton>
             }
             isOpen={isPopoverOpen}
+            repositionOnScroll={true}
           >
             <p>
               This is the popover content, notice how it can overflow the
               flyout!
             </p>
+            <p>
+              When placed in a flyout, the <EuiCode>repositionOnScroll</EuiCode>{' '}
+              prop ensures that the popover scrolls with body of the flyout.
+            </p>
           </EuiPopover>
           <EuiSpacer size="m" />
           <EuiForm component="form">
@@ -221,6 +227,7 @@ export default () => {
                 valueOfSelected={superSelectvalue}
                 onChange={(value) => onSuperSelectChange(value)}
                 itemLayoutAlign="top"
+                repositionOnScroll={true}
                 hasDividers
               />
             </EuiFormRow>
@@ -229,6 +236,7 @@ export default () => {
           <EuiPopover
             isOpen={isExpressionOpen}
             closePopover={() => setIsExpressionOpen(false)}
+            repositionOnScroll={true}
             button={
               <EuiExpression
                 description="expression"
diff --git a/src/components/form/super_select/super_select.tsx b/src/components/form/super_select/super_select.tsx
index bba1e11e6d2..19bb918f84c 100644
--- a/src/components/form/super_select/super_select.tsx
+++ b/src/components/form/super_select/super_select.tsx
@@ -77,6 +77,14 @@ export type EuiSuperSelectProps<T extends string> = CommonProps &
      * Controls whether the options are shown. Default: false
      */
     isOpen?: boolean;
+
+    /**
+     * When `true`, the popover's position is re-calculated when the user
+     * scrolls, this supports having fixed-position popover anchors. This value is passed
+     * to the EuiInputPopover component. When nesting an `EuiSuperSelect` in a scrollable container,
+     * `repositionOnScroll` should be `true`
+     */
+    repositionOnScroll?: boolean;
   };
 
 export class EuiSuperSelect<T extends string> extends Component<
@@ -252,6 +260,7 @@ export class EuiSuperSelect<T extends string> extends Component<
       fullWidth,
       popoverClassName,
       compressed,
+      repositionOnScroll,
       ...rest
     } = this.props;
 
@@ -318,6 +327,7 @@ export class EuiSuperSelect<T extends string> extends Component<
         closePopover={this.closePopover}
         panelPaddingSize="none"
         fullWidth={fullWidth}
+        repositionOnScroll={repositionOnScroll}
       >
         <EuiScreenReaderOnly>
           <p role="alert">
diff --git a/src/components/popover/popover.tsx b/src/components/popover/popover.tsx
index 5957c52e8a4..922e66e1464 100644
--- a/src/components/popover/popover.tsx
+++ b/src/components/popover/popover.tsx
@@ -151,7 +151,8 @@ export interface EuiPopoverProps {
   popoverRef?: Ref<HTMLDivElement>;
   /**
    * When `true`, the popover's position is re-calculated when the user
-   * scrolls, this supports having fixed-position popover anchors
+   * scrolls, this supports having fixed-position popover anchors. When nesting
+   * an `EuiPopover` in a scrollable container, `repositionOnScroll` should be `true`
    */
   repositionOnScroll?: boolean;
   /**
@@ -510,7 +511,7 @@ export class EuiPopover extends Component<Props, State> {
     }
 
     if (this.props.repositionOnScroll) {
-      window.addEventListener('scroll', this.positionPopoverFixed);
+      window.addEventListener('scroll', this.positionPopoverFixed, true);
     }
   }
 
@@ -523,9 +524,9 @@ export class EuiPopover extends Component<Props, State> {
     // update scroll listener
     if (prevProps.repositionOnScroll !== this.props.repositionOnScroll) {
       if (this.props.repositionOnScroll) {
-        window.addEventListener('scroll', this.positionPopoverFixed);
+        window.addEventListener('scroll', this.positionPopoverFixed, true);
       } else {
-        window.removeEventListener('scroll', this.positionPopoverFixed);
+        window.removeEventListener('scroll', this.positionPopoverFixed, true);
       }
     }