diff --git a/CHANGELOG.md b/CHANGELOG.md
index 85c7bbe03c2..ec90aef2999 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -2,6 +2,7 @@
 
 - Updated `EuiRangeLevel` `color` property to accept CSS color values ([#5171](https://github.com/elastic/eui/pull/5171))
 - Added optional visual line highlighting to `EuiCodeBlock` ([#5207](https://github.com/elastic/eui/pull/5207))
+- Added `popoverProps` to `EuiSuperSelect` and deprecated `popoverClassName` & `repositionOnScroll` ([#5214](https://github.com/elastic/eui/pull/5214))
 
 **Bug fixes**
 
diff --git a/src/components/form/super_select/__snapshots__/super_select.test.tsx.snap b/src/components/form/super_select/__snapshots__/super_select.test.tsx.snap
index 70e22522b7b..b210918e653 100644
--- a/src/components/form/super_select/__snapshots__/super_select.test.tsx.snap
+++ b/src/components/form/super_select/__snapshots__/super_select.test.tsx.snap
@@ -703,6 +703,233 @@ exports[`EuiSuperSelect props options are rendered when select is open 1`] = `
 </div>
 `;
 
+exports[`EuiSuperSelect props renders popoverProps on the underlying EuiPopover 1`] = `
+<EuiSuperSelect
+  compressed={false}
+  fullWidth={false}
+  hasDividers={false}
+  isInvalid={false}
+  isLoading={false}
+  onChange={[Function]}
+  options={
+    Array [
+      Object {
+        "inputDisplay": "Option #1",
+        "value": "1",
+      },
+      Object {
+        "inputDisplay": "Option #2",
+        "value": "2",
+      },
+    ]
+  }
+  popoverProps={
+    Object {
+      "className": "goes-on-outermost-wrapper",
+      "panelClassName": "goes-on-popover-panel",
+      "repositionOnScroll": true,
+    }
+  }
+  valueOfSelected="2"
+>
+  <EuiInputPopover
+    anchorPosition="downLeft"
+    attachToAnchor={true}
+    className="euiSuperSelect goes-on-outermost-wrapper"
+    closePopover={[Function]}
+    display="block"
+    fullWidth={false}
+    input={
+      <EuiSuperSelectControl
+        className=""
+        compressed={false}
+        fullWidth={false}
+        isInvalid={false}
+        isLoading={false}
+        onClick={[Function]}
+        onKeyDown={[Function]}
+        options={
+          Array [
+            Object {
+              "inputDisplay": "Option #1",
+              "value": "1",
+            },
+            Object {
+              "inputDisplay": "Option #2",
+              "value": "2",
+            },
+          ]
+        }
+        value="2"
+      />
+    }
+    isOpen={false}
+    panelClassName="goes-on-popover-panel"
+    panelPaddingSize="none"
+    repositionOnScroll={true}
+  >
+    <EuiPopover
+      anchorPosition="downLeft"
+      attachToAnchor={true}
+      button={
+        <EuiResizeObserver
+          onResize={[Function]}
+        >
+          [Function]
+        </EuiResizeObserver>
+      }
+      buttonRef={[Function]}
+      className="euiInputPopover euiSuperSelect goes-on-outermost-wrapper"
+      closePopover={[Function]}
+      display="block"
+      hasArrow={true}
+      isOpen={false}
+      ownFocus={false}
+      panelClassName="goes-on-popover-panel"
+      panelPaddingSize="none"
+      panelRef={[Function]}
+      repositionOnScroll={true}
+    >
+      <EuiOutsideClickDetector
+        onOutsideClick={[Function]}
+      >
+        <div
+          className="euiPopover euiPopover--anchorDownLeft euiPopover--displayBlock euiInputPopover euiSuperSelect goes-on-outermost-wrapper"
+          onKeyDown={[Function]}
+          onMouseDown={[Function]}
+          onMouseUp={[Function]}
+          onTouchEnd={[Function]}
+          onTouchStart={[Function]}
+        >
+          <div
+            className="euiPopover__anchor"
+          >
+            <EuiResizeObserver
+              onResize={[Function]}
+            >
+              <div>
+                <EuiSuperSelectControl
+                  className=""
+                  compressed={false}
+                  fullWidth={false}
+                  isInvalid={false}
+                  isLoading={false}
+                  onClick={[Function]}
+                  onKeyDown={[Function]}
+                  options={
+                    Array [
+                      Object {
+                        "inputDisplay": "Option #1",
+                        "value": "1",
+                      },
+                      Object {
+                        "inputDisplay": "Option #2",
+                        "value": "2",
+                      },
+                    ]
+                  }
+                  value="2"
+                >
+                  <input
+                    type="hidden"
+                    value="2"
+                  />
+                  <EuiFormControlLayout
+                    compressed={false}
+                    fullWidth={false}
+                    icon={
+                      Object {
+                        "side": "right",
+                        "type": "arrowDown",
+                      }
+                    }
+                    isLoading={false}
+                  >
+                    <div
+                      className="euiFormControlLayout"
+                    >
+                      <div
+                        className="euiFormControlLayout__childrenWrapper"
+                      >
+                        <EuiScreenReaderOnly>
+                          <span
+                            className="euiScreenReaderOnly"
+                            id="generated-id"
+                          >
+                            <EuiI18n
+                              default="Select an option: {selectedValue}, is selected"
+                              token="euiSuperSelectControl.selectAnOption"
+                              values={
+                                Object {
+                                  "selectedValue": "Option #2",
+                                }
+                              }
+                            >
+                              Select an option: Option #2, is selected
+                            </EuiI18n>
+                          </span>
+                        </EuiScreenReaderOnly>
+                        <button
+                          aria-haspopup="true"
+                          aria-labelledby="generated-id"
+                          className="euiSuperSelectControl"
+                          onClick={[Function]}
+                          onKeyDown={[Function]}
+                          type="button"
+                        >
+                          Option #2
+                        </button>
+                        <EuiFormControlLayoutIcons
+                          compressed={false}
+                          icon={
+                            Object {
+                              "side": "right",
+                              "type": "arrowDown",
+                            }
+                          }
+                          isLoading={false}
+                        >
+                          <div
+                            className="euiFormControlLayoutIcons euiFormControlLayoutIcons--right"
+                          >
+                            <EuiFormControlLayoutCustomIcon
+                              size="m"
+                              type="arrowDown"
+                            >
+                              <span
+                                className="euiFormControlLayoutCustomIcon"
+                              >
+                                <EuiIcon
+                                  aria-hidden="true"
+                                  className="euiFormControlLayoutCustomIcon__icon"
+                                  size="m"
+                                  type="arrowDown"
+                                >
+                                  <span
+                                    aria-hidden="true"
+                                    className="euiFormControlLayoutCustomIcon__icon"
+                                    data-euiicon-type="arrowDown"
+                                    size="m"
+                                  />
+                                </EuiIcon>
+                              </span>
+                            </EuiFormControlLayoutCustomIcon>
+                          </div>
+                        </EuiFormControlLayoutIcons>
+                      </div>
+                    </div>
+                  </EuiFormControlLayout>
+                </EuiSuperSelectControl>
+              </div>
+            </EuiResizeObserver>
+          </div>
+        </div>
+      </EuiOutsideClickDetector>
+    </EuiPopover>
+  </EuiInputPopover>
+</EuiSuperSelect>
+`;
+
 exports[`EuiSuperSelect props select component is rendered 1`] = `
 <div
   class="euiPopover euiPopover--anchorDownLeft euiPopover--displayBlock euiInputPopover euiSuperSelect"
diff --git a/src/components/form/super_select/super_select.test.tsx b/src/components/form/super_select/super_select.test.tsx
index b11e66dd879..afd2212e885 100644
--- a/src/components/form/super_select/super_select.test.tsx
+++ b/src/components/form/super_select/super_select.test.tsx
@@ -161,5 +161,22 @@ describe('EuiSuperSelect', () => {
 
       expect(takeMountedSnapshot(component)).toMatchSnapshot();
     });
+
+    test('renders popoverProps on the underlying EuiPopover', () => {
+      const component = mount(
+        <EuiSuperSelect
+          options={options}
+          valueOfSelected="2"
+          onChange={() => {}}
+          popoverProps={{
+            className: 'goes-on-outermost-wrapper',
+            panelClassName: 'goes-on-popover-panel',
+            repositionOnScroll: true,
+          }}
+        />
+      );
+
+      expect(component).toMatchSnapshot();
+    });
   });
 });
diff --git a/src/components/form/super_select/super_select.tsx b/src/components/form/super_select/super_select.tsx
index 19bb918f84c..2f91b0e1253 100644
--- a/src/components/form/super_select/super_select.tsx
+++ b/src/components/form/super_select/super_select.tsx
@@ -17,7 +17,7 @@ import {
   EuiSuperSelectControlProps,
   EuiSuperSelectOption,
 } from './super_select_control';
-import { EuiInputPopover } from '../../popover';
+import { EuiInputPopover, EuiPopoverProps } from '../../popover';
 import {
   EuiContextMenuItem,
   EuiContextMenuItemLayoutAlignment,
@@ -69,20 +69,34 @@ export type EuiSuperSelectProps<T extends string> = CommonProps &
     itemLayoutAlign?: EuiContextMenuItemLayoutAlignment;
 
     /**
-     * Applied to the outermost wrapper (popover)
+     * Controls whether the options are shown. Default: false
      */
-    popoverClassName?: string;
+    isOpen?: boolean;
 
     /**
-     * Controls whether the options are shown. Default: false
+     * Optional props to pass to the underlying [EuiPopover](/#/layout/popover).
+     *  Allows fine-grained control of the popover dropdown menu, including
+     * `repositionOnScroll` for EuiSuperSelects used within scrollable containers,
+     * and customizing popover panel styling.
+     *
+     * Does not accept a nested `popoverProps.isOpen` property - use the top level
+     * `isOpen` API instead.
      */
-    isOpen?: boolean;
+    popoverProps?: Partial<CommonProps & Omit<EuiPopoverProps, 'isOpen'>>;
+
+    /**
+     * Applied to the outermost wrapper (popover)
+     *
+     * **DEPRECATED: Use `popoverProps.className` instead (will take precedence over this prop if set).**
+     */
+    popoverClassName?: string;
 
     /**
      * 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,
+     * scrolls. When nesting an `EuiSuperSelect` in a scrollable container,
      * `repositionOnScroll` should be `true`
+     *
+     * **DEPRECATED: Use `popoverProps.repositionOnScroll` instead (will take precedence over this prop if set).**
      */
     repositionOnScroll?: boolean;
   };
@@ -259,12 +273,16 @@ export class EuiSuperSelect<T extends string> extends Component<
       itemLayoutAlign,
       fullWidth,
       popoverClassName,
+      popoverProps,
       compressed,
       repositionOnScroll,
       ...rest
     } = this.props;
 
-    const popoverClasses = classNames('euiSuperSelect', popoverClassName);
+    const popoverClasses = classNames(
+      'euiSuperSelect',
+      popoverProps?.className ?? popoverClassName
+    );
 
     const buttonClasses = classNames(
       {
@@ -321,13 +339,14 @@ export class EuiSuperSelect<T extends string> extends Component<
 
     return (
       <EuiInputPopover
-        className={popoverClasses}
-        input={button}
-        isOpen={isOpen || this.state.isPopoverOpen}
         closePopover={this.closePopover}
         panelPaddingSize="none"
-        fullWidth={fullWidth}
         repositionOnScroll={repositionOnScroll}
+        {...popoverProps}
+        className={popoverClasses}
+        isOpen={isOpen || this.state.isPopoverOpen}
+        input={button}
+        fullWidth={fullWidth}
       >
         <EuiScreenReaderOnly>
           <p role="alert">