diff --git a/src/components/Popover/Popover.jsx b/src/components/Popover/Popover.jsx
index d0d24768..f0f0acfd 100644
--- a/src/components/Popover/Popover.jsx
+++ b/src/components/Popover/Popover.jsx
@@ -12,24 +12,40 @@ export const Popover = React.forwardRef((props, ref) => {
   const {
     placement,
     children,
+    popoverTargetId,
     portalId,
     ...restProps
   } = props;
 
   const PopoverEl = (
-    <div
-      {...transferProps(restProps)}
-      className={classNames(
-        styles.root,
-        ref && styles.isRootControlled,
-        getRootSideClassName(placement, styles),
-        getRootAlignmentClassName(placement, styles),
+    <>
+      {/**
+        * This hack is needed because the default behavior of the Popover API is to place the popover into a
+        * top-layer. It is currently not possible to position an element in the top-layer relative to a normal element.
+        * This will create a hidden browser popover, then with CSS it will open and close the RUI popover.
+        */}
+      {!!popoverTargetId && (
+        <div
+          className={styles.helper}
+          id={popoverTargetId}
+          popover="auto"
+        />
       )}
-      ref={ref}
-    >
-      {children}
-      <span className={styles.arrow} />
-    </div>
+      <div
+        {...transferProps(restProps)}
+        className={classNames(
+          styles.root,
+          ref && styles.isRootControlled,
+          popoverTargetId && styles.controlledPopover,
+          getRootSideClassName(placement, styles),
+          getRootAlignmentClassName(placement, styles),
+        )}
+        ref={ref}
+      >
+        {children}
+        <span className={styles.arrow} />
+      </div>
+    </>
   );
 
   if (portalId === null) {
@@ -41,6 +57,7 @@ export const Popover = React.forwardRef((props, ref) => {
 
 Popover.defaultProps = {
   placement: 'bottom',
+  popoverTargetId: null,
   portalId: null,
 };
 
@@ -67,6 +84,12 @@ Popover.propTypes = {
     'left-start',
     'left-end',
   ]),
+  /**
+   * If set, the popover will become controlled, meaning it will be hidden by default and will need a trigger to open.
+   * This sets the ID of the internal helper element for the popover.
+   * Assign the same ID to `popovertarget` of a trigger to make it open and close.
+   */
+  popoverTargetId: PropTypes.string,
   /**
    * If set, popover is rendered in the React Portal with that ID.
    */
diff --git a/src/components/Popover/Popover.module.scss b/src/components/Popover/Popover.module.scss
index 1c3d1873..b9b554be 100644
--- a/src/components/Popover/Popover.module.scss
+++ b/src/components/Popover/Popover.module.scss
@@ -1,6 +1,12 @@
-// 1. Reset positioning for controlled variant.
-// 2. Shift Popover so there is space for the arrow between Popover and reference element.
-// 3. Add top offset in case it's not defined by external library.
+// 1. Hide the popover by default. This is needed because the popover is
+//    controlled via CSS with the help of the helper popover. The popover can't
+//    be displayed directly, because relative positioning doesn't work with
+//    elements on the top-layer, so this CSS hack is needed.
+// 2. Hide the popover helper element.
+// 3. If the popover helper is open, show the actual popover.
+// 4. Reset positioning for controlled variant.
+// 5. Shift Popover so there is space for the arrow between Popover and reference element.
+// 6. Add top offset in case it's not defined by external library.
 
 @use "theme";
 
@@ -49,6 +55,28 @@
         }
     }
 
+    // Controlled popover
+    .controlledPopover {
+        display: none; // 1.
+    }
+
+    .helper {
+        position: fixed; // 2.
+        inset: unset;
+        top: 0;
+        right: 0;
+        width: auto;
+        height: auto;
+        padding: 0;
+        border: none;
+        background: transparent;
+        pointer-events: none;
+    }
+
+    .helper:popover-open ~ .controlledPopover {
+        display: block; // 3.
+    }
+
     // Sides
     .isRootAtTop {
         bottom: calc(100% + #{theme.$arrow-gap} - #{theme.$arrow-safe-rendering-overlap});
@@ -212,27 +240,27 @@
     .isRootControlled.isRootAtBottom,
     .isRootControlled.isRootAtLeft,
     .isRootControlled.isRootAtRight {
-        inset: unset; // 1.
+        inset: unset; // 4.
     }
 
     .isRootControlled.isRootAtTop {
-        transform: translate(0, calc(-1 * #{theme.$arrow-height})); // 2.
+        transform: translate(0, calc(-1 * #{theme.$arrow-height})); // 5.
     }
 
     .isRootControlled.isRootAtBottom {
-        transform: translate(0, #{theme.$arrow-height}); // 2.
+        transform: translate(0, #{theme.$arrow-height}); // 5.
     }
 
     .isRootControlled.isRootAtLeft {
-        transform: translate(calc(-1 * #{theme.$arrow-height}), 0); // 2.
+        transform: translate(calc(-1 * #{theme.$arrow-height}), 0); // 5.
     }
 
     .isRootControlled.isRootAtRight {
-        transform: translate(#{theme.$arrow-height}, 0); // 2.
+        transform: translate(#{theme.$arrow-height}, 0); // 5.
     }
 
     .isRootControlled.isRootAtLeft.isRootAtStart,
     .isRootControlled.isRootAtRight.isRootAtStart {
-        top: 0; // 3.
+        top: 0; // 6.
     }
 }
diff --git a/src/components/Popover/README.md b/src/components/Popover/README.md
index dac06ce8..46f98c9a 100644
--- a/src/components/Popover/README.md
+++ b/src/components/Popover/README.md
@@ -284,6 +284,39 @@ React.createElement(() => {
 });
 ```
 
+## Controlled Popover
+
+Popover API can be used to control visibility of Popover component. You need to
+set `id` on the trigger element and matching `popoverTargetId` attribute on the
+Popover component. This leverages the browser's Popover API to control the
+popover, automatically closing it when the trigger or the backdrop is pressed.
+
+```docoff-react-preview
+React.createElement(() => {
+  // All inline styles in this example are for demonstration purposes only.
+  return (
+    <div
+      style={{
+        display: 'grid',
+        placeContent: 'center',
+        minWidth: '20rem',
+        minHeight: '10rem',
+      }}
+    >
+      <PopoverWrapper>
+        <Button
+          label="Want to see a popover? Click me!"
+          popovertarget="my-popover-helper"
+        />
+        <Popover id="my-popover" popoverTargetId="my-popover-helper">
+            Hello there!
+        </Popover>
+      </PopoverWrapper>
+    </div>
+  );
+});
+```
+
 ## Forwarding HTML Attributes
 
 In addition to the options below in the [component's API](#api) section, you