diff --git a/packages/react-components/react-search/etc/react-search.api.md b/packages/react-components/react-search/etc/react-search.api.md
index 35e030a97c5b08..10d58a3c439ee9 100644
--- a/packages/react-components/react-search/etc/react-search.api.md
+++ b/packages/react-components/react-search/etc/react-search.api.md
@@ -35,7 +35,9 @@ export type SearchBoxSlots = {
 };
 
 // @public
-export type SearchBoxState = ComponentState<SearchBoxSlots> & Required<Pick<InputState, 'size'>> & Required<Pick<SearchBoxProps, 'disabled'>>;
+export type SearchBoxState = ComponentState<SearchBoxSlots> & Required<Pick<InputState, 'size'>> & Required<Pick<SearchBoxProps, 'disabled'>> & {
+    focused: boolean;
+};
 
 // @public
 export const useSearchBox_unstable: (props: SearchBoxProps, ref: React_2.Ref<HTMLInputElement>) => SearchBoxState;
diff --git a/packages/react-components/react-search/src/components/SearchBox/SearchBox.types.ts b/packages/react-components/react-search/src/components/SearchBox/SearchBox.types.ts
index 9716052f4899cc..e7589a14f1058c 100644
--- a/packages/react-components/react-search/src/components/SearchBox/SearchBox.types.ts
+++ b/packages/react-components/react-search/src/components/SearchBox/SearchBox.types.ts
@@ -22,4 +22,6 @@ export type SearchBoxProps = ComponentProps<SearchBoxSlots>;
  */
 export type SearchBoxState = ComponentState<SearchBoxSlots> &
   Required<Pick<InputState, 'size'>> &
-  Required<Pick<SearchBoxProps, 'disabled'>>;
+  Required<Pick<SearchBoxProps, 'disabled'>> & {
+    focused: boolean;
+  };
diff --git a/packages/react-components/react-search/src/components/SearchBox/__snapshots__/SearchBox.test.tsx.snap b/packages/react-components/react-search/src/components/SearchBox/__snapshots__/SearchBox.test.tsx.snap
index ff04dd5806b3ff..e20a9e1b847ed7 100644
--- a/packages/react-components/react-search/src/components/SearchBox/__snapshots__/SearchBox.test.tsx.snap
+++ b/packages/react-components/react-search/src/components/SearchBox/__snapshots__/SearchBox.test.tsx.snap
@@ -35,6 +35,7 @@ exports[`SearchBox renders a default state 1`] = `
         aria-label="clear"
         class="fui-SearchBox__dismiss"
         role="button"
+        tabindex="-1"
       >
         <svg
           aria-hidden="true"
diff --git a/packages/react-components/react-search/src/components/SearchBox/useSearchBox.tsx b/packages/react-components/react-search/src/components/SearchBox/useSearchBox.tsx
index 788018286e9097..b6794c9b37bcb0 100644
--- a/packages/react-components/react-search/src/components/SearchBox/useSearchBox.tsx
+++ b/packages/react-components/react-search/src/components/SearchBox/useSearchBox.tsx
@@ -1,6 +1,12 @@
 import * as React from 'react';
-import { mergeCallbacks, resolveShorthand, useControllableState, useEventCallback } from '@fluentui/react-utilities';
-import { Input } from '@fluentui/react-input';
+import {
+  mergeCallbacks,
+  resolveShorthand,
+  useControllableState,
+  useEventCallback,
+  useMergedRefs,
+} from '@fluentui/react-utilities';
+import { Input, InputState } from '@fluentui/react-input';
 import type { SearchBoxProps, SearchBoxState } from './SearchBox.types';
 import { DismissRegular, SearchRegular } from '@fluentui/react-icons';
 
@@ -14,7 +20,10 @@ import { DismissRegular, SearchRegular } from '@fluentui/react-icons';
  * @param ref - reference to root HTMLElement of SearchBox
  */
 export const useSearchBox_unstable = (props: SearchBoxProps, ref: React.Ref<HTMLInputElement>): SearchBoxState => {
-  const { size = 'medium', disabled = false, contentBefore, dismiss, contentAfter, ...inputProps } = props;
+  const { size = 'medium', disabled = false, root, contentBefore, dismiss, contentAfter, ...inputProps } = props;
+
+  const searchBoxRootRef = React.useRef<HTMLDivElement>(null);
+  const searchBoxRef = React.useRef<HTMLInputElement>(null);
 
   const [value, setValue] = useControllableState({
     state: props.value,
@@ -22,6 +31,17 @@ export const useSearchBox_unstable = (props: SearchBoxProps, ref: React.Ref<HTML
     initialState: '',
   });
 
+  // Tracks the focus of the component for the contentAfter and dismiss button
+  const [focused, setFocused] = React.useState(false);
+
+  const onFocus = useEventCallback(() => {
+    setFocused(true);
+  });
+
+  const onBlur: React.FocusEventHandler<HTMLSpanElement> = useEventCallback(ev => {
+    setFocused(!!searchBoxRootRef.current?.contains(ev.relatedTarget));
+  });
+
   const state: SearchBoxState = {
     components: {
       root: Input,
@@ -30,9 +50,12 @@ export const useSearchBox_unstable = (props: SearchBoxProps, ref: React.Ref<HTML
     },
 
     root: {
-      ref,
+      ref: useMergedRefs(searchBoxRef, ref),
       type: 'search',
       input: {}, // defining here to have access in styles hook
+
+      disabled,
+      size,
       value,
 
       contentBefore: resolveShorthand(contentBefore, {
@@ -44,6 +67,10 @@ export const useSearchBox_unstable = (props: SearchBoxProps, ref: React.Ref<HTML
 
       ...inputProps,
 
+      root: resolveShorthand(root, {
+        required: true,
+      }),
+
       onChange: useEventCallback(ev => {
         const newValue = ev.target.value;
         props.onChange?.(ev, { value: newValue });
@@ -55,15 +82,24 @@ export const useSearchBox_unstable = (props: SearchBoxProps, ref: React.Ref<HTML
         children: <DismissRegular />,
         role: 'button',
         'aria-label': 'clear',
+        tabIndex: -1,
       },
       required: true,
     }),
-    contentAfter: resolveShorthand(contentAfter, { required: true }),
+    contentAfter: resolveShorthand(contentAfter, {
+      required: true,
+    }),
 
     disabled,
+    focused,
     size,
   };
 
+  const searchBoxRoot = state.root.root as InputState['root'];
+  searchBoxRoot.ref = useMergedRefs(searchBoxRoot.ref, searchBoxRootRef);
+  searchBoxRoot.onFocus = useEventCallback(mergeCallbacks(searchBoxRoot.onFocus, onFocus));
+  searchBoxRoot.onBlur = useEventCallback(mergeCallbacks(searchBoxRoot.onBlur, onBlur));
+
   const onDismissClick = useEventCallback(mergeCallbacks(state.dismiss?.onClick, () => setValue('')));
   if (state.dismiss) {
     state.dismiss.onClick = onDismissClick;
diff --git a/packages/react-components/react-search/src/components/SearchBox/useSearchBoxStyles.styles.ts b/packages/react-components/react-search/src/components/SearchBox/useSearchBoxStyles.styles.ts
index e7817f6ee7610c..945322b7f02a41 100644
--- a/packages/react-components/react-search/src/components/SearchBox/useSearchBoxStyles.styles.ts
+++ b/packages/react-components/react-search/src/components/SearchBox/useSearchBoxStyles.styles.ts
@@ -39,14 +39,6 @@ const useRootStyles = makeStyles({
     paddingLeft: tokens.spacingHorizontalSNudge,
     paddingRight: 0,
 
-    // dismiss + contentAfter appear on focus
-    '& + span': {
-      display: 'none',
-    },
-    '&:focus + span': {
-      display: 'flex',
-    },
-
     // removes the WebKit pseudoelement styling
     '::-webkit-search-decoration': {
       display: 'none',
@@ -62,6 +54,11 @@ const useContentAfterStyles = makeStyles({
     paddingLeft: tokens.spacingHorizontalM,
     columnGap: tokens.spacingHorizontalXS,
   },
+  rest: {
+    opacity: 0,
+    height: 0,
+    width: 0,
+  },
 });
 
 const useDismissClassName = makeResetStyles({
@@ -93,7 +90,7 @@ const useDismissStyles = makeStyles({
  * Apply styling to the SearchBox slots based on the state
  */
 export const useSearchBoxStyles_unstable = (state: SearchBoxState): SearchBoxState => {
-  const { disabled, size } = state;
+  const { disabled, focused, size } = state;
 
   const rootStyles = useRootStyles();
   const contentAfterStyles = useContentAfterStyles();
@@ -109,14 +106,18 @@ export const useSearchBoxStyles_unstable = (state: SearchBoxState): SearchBoxSta
       dismissClassName,
       disabled && dismissStyles.disabled,
       dismissStyles[size],
+
       state.dismiss.className,
     );
   }
 
   if (state.contentAfter) {
-    state.contentAfter!.className = mergeClasses(
+    state.contentAfter.className = mergeClasses(
       searchBoxClassNames.contentAfter,
       contentAfterStyles.contentAfter,
+
+      !focused && contentAfterStyles.rest,
+
       state.contentAfter.className,
     );
   } else if (state.dismiss) {
diff --git a/packages/react-components/react-search/stories/SearchBox/SearchBoxDefault.stories.tsx b/packages/react-components/react-search/stories/SearchBox/SearchBoxDefault.stories.tsx
index fe7ab84e788d32..3f2478e58a6c71 100644
--- a/packages/react-components/react-search/stories/SearchBox/SearchBoxDefault.stories.tsx
+++ b/packages/react-components/react-search/stories/SearchBox/SearchBoxDefault.stories.tsx
@@ -3,4 +3,19 @@ import { SearchBox, SearchBoxProps } from '@fluentui/react-search';
 
 import { FilterRegular } from '@fluentui/react-icons';
 
-export const Default = (props: Partial<SearchBoxProps>) => <SearchBox {...props} contentAfter={<FilterRegular />} />;
+// TODO: split into different stories
+export const Default = (props: Partial<SearchBoxProps>) => (
+  <>
+    <SearchBox {...props} contentAfter={<FilterRegular />} size="small" placeholder="small" />
+    <SearchBox {...props} contentAfter={<FilterRegular />} size="medium" placeholder="medium" />
+    <SearchBox {...props} contentAfter={<FilterRegular />} size="large" placeholder="large" />
+    <SearchBox {...props} contentAfter={null} placeholder="no contentAfter" />
+    <SearchBox {...props} contentAfter={<FilterRegular />} disabled placeholder="disabled" />
+    <SearchBox
+      {...props}
+      contentAfter={<FilterRegular tabIndex={0} onClick={() => console.log('clicked')} />}
+      placeholder="contentAfter button"
+    />
+    <SearchBox root={{ onFocus: () => console.log('test') }} placeholder="custom onFocus" />
+  </>
+);
