diff --git a/src/components/input/SelectNext.tsx b/src/components/input/SelectNext.tsx
index 2cfb2127..4892930d 100644
--- a/src/components/input/SelectNext.tsx
+++ b/src/components/input/SelectNext.tsx
@@ -1,5 +1,5 @@
 import classnames from 'classnames';
-import type { ComponentChildren, RefObject } from 'preact';
+import type { ComponentChildren, JSX, RefObject } from 'preact';
 import {
   useCallback,
   useContext,
@@ -15,6 +15,7 @@ import { useFocusAway } from '../../hooks/use-focus-away';
 import { useKeyPress } from '../../hooks/use-key-press';
 import { useSyncedRef } from '../../hooks/use-synced-ref';
 import type { CompositeProps } from '../../types';
+import { ListenerCollection } from '../../util/listener-collection';
 import { downcastRef } from '../../util/typing';
 import { MenuCollapseIcon, MenuExpandIcon } from '../icons';
 import { inputGroupStyles } from './InputGroup';
@@ -103,38 +104,87 @@ function SelectOption<T>({
 
 SelectOption.displayName = 'SelectNext.Option';
 
-function useShouldDropUp(
+const LISTBOX_TOGGLE_GAP = '.25rem';
+const OPTION_SELECTOR = '[role="option"]:not([aria-disabled="true"])';
+
+function useListboxPositioning(
   buttonRef: RefObject<HTMLElement | undefined>,
   listboxRef: RefObject<HTMLElement | null>,
   listboxOpen: boolean,
-): boolean {
-  const [shouldListboxDropUp, setShouldListboxDropUp] = useState(false);
+  nativePopoverSupported: boolean,
+) {
+  const [positioningStyles, setPositioningStyles] = useState<
+    JSX.HTMLAttributes['style']
+  >({});
 
   useLayoutEffect(() => {
-    // Reset shouldListboxDropUp so that it does not affect calculations next
-    // time listbox opens
-    if (!buttonRef.current || !listboxRef.current || !listboxOpen) {
-      setShouldListboxDropUp(false);
-      return;
+    const listboxEl = listboxRef.current;
+    const buttonEl = buttonRef.current;
+
+    if (!buttonEl || !listboxEl || !listboxOpen) {
+      return () => {};
     }
 
+    const listeners = new ListenerCollection();
     const viewportHeight = window.innerHeight;
-    const { top: buttonDistanceToTop, bottom: buttonBottom } =
-      buttonRef.current.getBoundingClientRect();
+    const {
+      top: buttonDistanceToTop,
+      bottom: buttonBottom,
+      left: buttonLeft,
+      height: buttonHeight,
+      width: buttonWidth,
+    } = buttonEl.getBoundingClientRect();
     const buttonDistanceToBottom = viewportHeight - buttonBottom;
-    const { bottom: listboxBottom } =
-      listboxRef.current.getBoundingClientRect();
-    const listboxDistanceToBottom = viewportHeight - listboxBottom;
+    const { height: listboxHeight } = listboxEl.getBoundingClientRect();
 
     // The listbox should drop up only if there's not enough space below to
-    // fit it, and there's also more absolute space above than below
-    setShouldListboxDropUp(
-      listboxDistanceToBottom < 0 &&
-        buttonDistanceToTop > buttonDistanceToBottom,
-    );
-  }, [buttonRef, listboxRef, listboxOpen]);
-
-  return shouldListboxDropUp;
+    // fit it, and also, there's more absolute space above than below
+    const shouldListboxDropUp =
+      buttonDistanceToBottom < listboxHeight &&
+      buttonDistanceToTop > buttonDistanceToBottom;
+
+    if (!nativePopoverSupported) {
+      setPositioningStyles(
+        shouldListboxDropUp
+          ? { bottom: '100%', marginBottom: LISTBOX_TOGGLE_GAP }
+          : { top: '100%', marginTop: LISTBOX_TOGGLE_GAP },
+      );
+    } else {
+      const toggleHandler = (e: Event) => {
+        // e.newState determines if the element that toggled is transitioning to
+        // open or closed state
+        if (!(e instanceof ToggleEvent) || !e.newState) {
+          return;
+        }
+
+        // When native popover is supported, we disable the automatic focusing
+        // in useArrowKeyNavigation, so we need to manually focus first/active
+        // option after opening the dropdown
+        const el =
+          listboxEl.querySelector(`${OPTION_SELECTOR}[aria-selected="true"]`) ??
+          listboxEl.querySelector(OPTION_SELECTOR);
+        (el as HTMLElement | null)?.focus();
+      };
+      listeners.add(listboxEl, 'toggle', toggleHandler);
+
+      const { top: bodyTop } = document.body.getBoundingClientRect();
+      const absBodyTop = Math.abs(bodyTop);
+      setPositioningStyles({
+        top: shouldListboxDropUp
+          ? `calc(${absBodyTop + buttonDistanceToTop - listboxHeight}px - ${LISTBOX_TOGGLE_GAP})`
+          : `calc(${absBodyTop + buttonDistanceToTop + buttonHeight}px + ${LISTBOX_TOGGLE_GAP})`,
+        left: buttonLeft && `${buttonLeft}px`,
+        minWidth: buttonWidth && `${buttonWidth}px`,
+      });
+    }
+
+    return () => {
+      listeners.removeAll();
+      setPositioningStyles({});
+    };
+  }, [buttonRef, listboxRef, listboxOpen, nativePopoverSupported]);
+
+  return positioningStyles;
 }
 
 export type SelectProps<T> = CompositeProps & {
@@ -166,6 +216,9 @@ export type SelectProps<T> = CompositeProps & {
 
   'aria-label'?: string;
   'aria-labelledby'?: string;
+
+  /** Test seam */
+  nativePopoverSupported?: boolean;
 };
 
 function SelectMain<T>({
@@ -182,18 +235,31 @@ function SelectMain<T>({
   right = false,
   'aria-label': ariaLabel,
   'aria-labelledby': ariaLabelledBy,
+
+  /* istanbul ignore next - test seam */
+  nativePopoverSupported = 'popover' in document.body,
 }: SelectProps<T>) {
-  const [listboxOpen, setListboxOpen] = useState(false);
-  const closeListbox = useCallback(() => setListboxOpen(false), []);
   const wrapperRef = useRef<HTMLDivElement | null>(null);
   const listboxRef = useRef<HTMLUListElement | null>(null);
+  const [listboxOpen, setListboxOpen] = useState(false);
+  const toggleListbox = useCallback(
+    (open: boolean) => {
+      setListboxOpen(open);
+      if (nativePopoverSupported) {
+        listboxRef.current?.togglePopover(open);
+      }
+    },
+    [nativePopoverSupported],
+  );
+  const closeListbox = useCallback(() => toggleListbox(false), [toggleListbox]);
   const listboxId = useId();
   const buttonRef = useSyncedRef(elementRef);
   const defaultButtonId = useId();
-  const shouldListboxDropUp = useShouldDropUp(
+  const positioningStyles = useListboxPositioning(
     buttonRef,
     listboxRef,
     listboxOpen,
+    nativePopoverSupported,
   );
 
   const selectValue = useCallback(
@@ -213,9 +279,9 @@ function SelectMain<T>({
   useArrowKeyNavigation(listboxRef, {
     horizontal: false,
     loop: false,
-    autofocus: true,
+    autofocus: !nativePopoverSupported,
     containerVisible: listboxOpen,
-    selector: '[role="option"]:not([aria-disabled="true"])',
+    selector: OPTION_SELECTOR,
   });
 
   useLayoutEffect(() => {
@@ -257,11 +323,11 @@ function SelectMain<T>({
         aria-label={ariaLabel}
         aria-labelledby={ariaLabelledBy}
         ref={downcastRef(buttonRef)}
-        onClick={() => setListboxOpen(prev => !prev)}
+        onClick={() => toggleListbox(!listboxOpen)}
         onKeyDown={e => {
           if (e.key === 'ArrowDown' && !listboxOpen) {
             e.preventDefault();
-            setListboxOpen(true);
+            toggleListbox(true);
           }
         }}
         data-testid="select-toggle-button"
@@ -273,21 +339,22 @@ function SelectMain<T>({
       </button>
       <SelectContext.Provider value={{ selectValue, value }}>
         <ul
+          // @ts-expect-error Popover attribute not yet part of type
+          popover
           className={classnames(
-            'absolute z-5 min-w-full max-h-80 overflow-y-auto',
+            'absolute z-5 max-h-80 overflow-y-auto',
             'rounded border bg-white shadow hover:shadow-md focus-within:shadow-md',
-            {
-              'top-full mt-1': !shouldListboxDropUp,
-              'bottom-full mb-1': shouldListboxDropUp,
-              'right-0': right,
-
+            { 'right-0': right },
+            !nativePopoverSupported && {
               // Hiding instead of unmounting to
               // * Ensure screen readers detect button as a listbox handler
               // * Listbox size can be computed to correctly drop up or down
               hidden: !listboxOpen,
+              'min-w-full': true,
             },
             listboxClasses,
           )}
+          style={positioningStyles}
           role="listbox"
           ref={listboxRef}
           id={listboxId}