diff --git a/e2e-tests/playwright/specs/functional/channels/search/team_selector.spec.ts b/e2e-tests/playwright/specs/functional/channels/search/team_selector.spec.ts
index 9766877957..496c2a508f 100644
--- a/e2e-tests/playwright/specs/functional/channels/search/team_selector.spec.ts
+++ b/e2e-tests/playwright/specs/functional/channels/search/team_selector.spec.ts
@@ -3,18 +3,27 @@
 
 import {expect, test} from '@mattermost/playwright-lib';
 
-test('team selector must show all my teams', async ({pw}) => {
+test('team selector should not be visible if user belongs to only one team', async ({pw}) => {
+    // # Create a user with only one team
     const {adminClient, user, team} = await pw.initSetup();
 
-    // # create 2 more teams and add the user to them
-    const teams = [team];
-    for (let i = 0; i < 2; i++) {
-        const newTeam = await adminClient.createTeam(pw.random.team('team', 'Team', 'O', true));
-        await adminClient.addUsersToTeam(newTeam.id, [user.id]);
-        teams.push(newTeam);
-    }
+    // # Create a channel in the team
+    const channel = await adminClient.createChannel(
+        pw.random.channel({
+            teamId: team.id,
+            displayName: 'Test Channel',
+            name: 'test-channel',
+        }),
+    );
 
-    // # Log in a user in new browser context
+    // # Post a message in the channel
+    const message = 'test message for search';
+    await adminClient.createPost({
+        channel_id: channel.id,
+        message,
+    });
+
+    // # Log in as the user
     const {channelsPage} = await pw.testBrowser.login(user);
 
     // # Visit a default channel page
@@ -24,66 +33,154 @@ test('team selector must show all my teams', async ({pw}) => {
     // # Open the search UI
     await channelsPage.globalHeader.openSearch();
 
-    // * Check that the team selector is visible
+    // * Verify that the team selector is not visible in the search box
     const page = channelsPage.page;
-    await expect(page.getByTestId('searchTeamsSelectorMenuButton')).toBeVisible();
 
-    // # Click on the team selector
+    // Make sure the search box is open but doesn't have a team selector
+    await expect(page.locator('#searchBox')).toBeVisible();
+    await expect(page.getByTestId('searchTeamSelector')).not.toBeVisible();
+
+    // # Now search for the message to see search results
+    await page.locator('#searchBox input').fill(message);
+    await page.keyboard.press('Enter');
+
+    // # Wait for search results to load
+    await expect(page.locator('#searchContainer')).toBeVisible();
+
+    // * Verify the team selector is not visible in search results panel
+    await expect(page.locator('.team-selector-container')).not.toBeVisible();
+});
+
+test('team selector should be visible if user belongs to multiple teams', async ({pw}) => {
+    // # Create a user and admin client
+    const {adminClient, user, team} = await pw.initSetup();
+
+    // # Create a second team and add the user to it
+    const secondTeam = await adminClient.createTeam(pw.random.team('team', 'Team', 'O', true));
+    await adminClient.addUsersToTeam(secondTeam.id, [user.id]);
+
+    // # Create a channel in the first team
+    const channel = await adminClient.createChannel(
+        pw.random.channel({
+            teamId: team.id,
+            displayName: 'Test Channel',
+            name: 'test-channel-multi',
+        }),
+    );
+
+    // # Post a message in the channel
+    const message = 'test message for multiple teams search';
+    await adminClient.createPost({
+        channel_id: channel.id,
+        message,
+    });
+
+    // # Log in as the user
+    const {channelsPage} = await pw.testBrowser.login(user);
+
+    // # Visit a default channel page
+    await channelsPage.goto(team.name);
+    await channelsPage.toBeVisible();
+
+    // # Open the search UI
+    await channelsPage.globalHeader.openSearch();
+
+    // * Verify that the team selector is visible in the search box
+    const page = channelsPage.page;
+
+    // Make sure the search box is open and has a team selector
+    await expect(page.locator('#searchBox')).toBeVisible();
+    await expect(page.getByTestId('searchTeamSelector')).toBeVisible();
+
+    // # Click on the team selector button
     await page.getByTestId('searchTeamsSelectorMenuButton').click();
 
-    // * Check that the team selector is visible
+    // * Verify that both teams are visible in the menu
     const teamSelector = page.getByRole('menu', {name: 'Select team'});
     await expect(teamSelector).toBeVisible();
-    // * Check that the team selector has the 3 teams
-    teams.forEach(async (t) => {
-        await expect(teamSelector.getByText(t.display_name)).toBeVisible();
-    });
-    // * Check that All teams is also visible
+    await expect(teamSelector.getByText(team.display_name)).toBeVisible();
+    await expect(teamSelector.getByText(secondTeam.display_name)).toBeVisible();
     await expect(teamSelector.getByText('All teams')).toBeVisible();
-    // * No <input> should be visible in the menu
-    await expect(teamSelector.getByLabel('Search teams')).not.toBeVisible();
 
-    // now create and join 3 more teams
-    for (let i = 0; i < 3; i++) {
+    // # Now search for the message to see search results
+    await page.click('body', {position: {x: 0, y: 0}}); // Click away to close team selector
+    await page.locator('#searchBox input').fill(message);
+    await page.keyboard.press('Enter');
+
+    // # Wait for search results to load
+    await expect(page.locator('#searchContainer')).toBeVisible();
+
+    // * Verify the team selector is visible in search results panel
+    await expect(page.locator('.team-selector-container')).toBeVisible();
+
+    // # Click on the team selector in results panel
+    await page.locator('.team-selector-container .search-teams-selector-menu-button').click();
+
+    // * Verify that both teams are visible in the results panel team selector
+    const resultsTeamSelector = page.getByRole('menu', {name: 'Select team'});
+    await expect(resultsTeamSelector).toBeVisible();
+    await expect(resultsTeamSelector.getByText(team.display_name)).toBeVisible();
+    await expect(resultsTeamSelector.getByText(secondTeam.display_name)).toBeVisible();
+    await expect(resultsTeamSelector.getByText('All teams')).toBeVisible();
+});
+
+test('team selector should show filter input with more than 4 teams', async ({pw}) => {
+    // # Create a user and admin client
+    const {adminClient, user, team} = await pw.initSetup();
+
+    // # Create 4 more teams (for a total of 5) and add the user to them
+    const teams = [team];
+    for (let i = 0; i < 4; i++) {
         const newTeam = await adminClient.createTeam(pw.random.team('team', 'Team', 'O', true));
         await adminClient.addUsersToTeam(newTeam.id, [user.id]);
         teams.push(newTeam);
     }
 
-    // refresh the page
+    // # Log in as the user
+    const {channelsPage} = await pw.testBrowser.login(user);
+
+    // # Visit a default channel page
     await channelsPage.goto(team.name);
+    await channelsPage.toBeVisible();
 
     // # Open the search UI
     await channelsPage.globalHeader.openSearch();
 
-    // # Click on the team selector
+    // # Verify team selector is visible and click on it
+    const page = channelsPage.page;
+    await expect(page.getByTestId('searchTeamSelector')).toBeVisible();
     await page.getByTestId('searchTeamsSelectorMenuButton').click();
 
-    // * Check that the team selector is visible
+    // # Verify the team filter input is visible with 5 teams
+    const teamSelector = page.getByRole('menu', {name: 'Select team'});
     await expect(teamSelector).toBeVisible();
-    // * Check that the team selector has the 6 teams
-    teams.forEach(async (t) => {
-        await expect(teamSelector.getByText(t.display_name)).toBeVisible();
-    });
-    // * Check that All teams is also visible
-    await expect(teamSelector.getByText('All teams')).toBeVisible();
-
-    // because there's more than 4 teams, the filter input should be visible
     await expect(teamSelector.getByLabel('Search teams')).toBeVisible();
 
-    // # Type the name of the first team
-    await page.getByLabel('Search teams').fill(teams[3].display_name);
+    // # Verify all teams are visible initially
+    for (const t of teams) {
+        await expect(teamSelector.getByText(t.display_name)).toBeVisible();
+    }
 
-    // * Check that the team selector is visible
-    await expect(teamSelector).toBeVisible();
+    // # Type filter text to match only one team
+    await teamSelector.getByLabel('Search teams').fill(teams[2].display_name);
 
-    // * Noew team [0] and [3] should be visible - 0 is visible because it was currently selected.
-    await expect(teamSelector.getByText(teams[0].display_name)).toBeVisible();
-    await expect(teamSelector.getByText(teams[3].display_name)).toBeVisible();
-    // * Check that All teams is also visible
-    await expect(teamSelector.getByText('All teams')).toBeVisible();
-    // * Check that the other teams are not visible
-    teams.slice(1, 3).forEach(async (t) => {
-        await expect(teamSelector.getByText(t.display_name)).not.toBeVisible();
-    });
+    // # Verify only the matching team is visible (and the currently selected team)
+    await expect(teamSelector.getByText(teams[0].display_name)).toBeVisible(); // Current team always visible
+    await expect(teamSelector.getByText(teams[2].display_name)).toBeVisible(); // Filtered team
+
+    // # Verify other teams are hidden
+    for (let i = 1; i < teams.length; i++) {
+        if (i !== 2) {
+            // Skip the filtered team we're expecting to see
+            await expect(teamSelector.getByText(teams[i].display_name)).not.toBeVisible();
+        }
+    }
+
+    // # Clear the filter
+    await teamSelector.getByLabel('Search teams').fill('');
+
+    // # Verify all teams are visible again
+    for (const t of teams) {
+        await expect(teamSelector.getByText(t.display_name)).toBeVisible();
+    }
 });
diff --git a/webapp/channels/src/components/new_search/new_search.tsx b/webapp/channels/src/components/new_search/new_search.tsx
index caae68caad..9964aff21d 100644
--- a/webapp/channels/src/components/new_search/new_search.tsx
+++ b/webapp/channels/src/components/new_search/new_search.tsx
@@ -9,7 +9,7 @@ import styled from 'styled-components';
 import {TrackCrossTeamSearchFeature, TrackCrossTeamSearchAllTeamsEvent, TrackCrossTeamSearchCurrentTeamEvent, TrackCrossTeamSearchDifferentTeamEvent} from 'mattermost-redux/constants/telemetry';
 import {getCurrentChannelNameForSearchShortcut} from 'mattermost-redux/selectors/entities/channels';
 import {getIsCrossTeamSearchEnabled} from 'mattermost-redux/selectors/entities/general';
-import {getCurrentTeamId} from 'mattermost-redux/selectors/entities/teams';
+import {getCurrentTeamId, getMyTeams} from 'mattermost-redux/selectors/entities/teams';
 
 import {trackFeatureEvent} from 'actions/telemetry_actions';
 import {updateSearchTerms, showSearchResults, updateSearchType, updateSearchTeam} from 'actions/views/rhs';
@@ -114,6 +114,7 @@ const NewSearch = (): JSX.Element => {
     const pluginSearch = useSelector(getSearchButtons);
     const currentTeamId = useSelector(getCurrentTeamId);
     const crossTeamSearchEnabled = useSelector(getIsCrossTeamSearchEnabled);
+    const myTeams = useSelector(getMyTeams);
 
     const dispatch = useDispatch();
     const [focused, setFocused] = useState<boolean>(false);
@@ -318,6 +319,7 @@ const NewSearch = (): JSX.Element => {
                         initialSearchType={searchType}
                         initialSearchTeam={searchTeam}
                         crossTeamSearchEnabled={crossTeamSearchEnabled}
+                        myTeams={myTeams}
                     />
                 </PopoverStyled>
             )}
diff --git a/webapp/channels/src/components/new_search/search_box.test.tsx b/webapp/channels/src/components/new_search/search_box.test.tsx
index 354db5fcac..8bfa5ee387 100644
--- a/webapp/channels/src/components/new_search/search_box.test.tsx
+++ b/webapp/channels/src/components/new_search/search_box.test.tsx
@@ -3,6 +3,8 @@
 
 import React from 'react';
 
+import type {Team} from '@mattermost/types/teams';
+
 import {
     renderWithContext,
     screen,
@@ -19,6 +21,7 @@ describe('components/new_search/SearchBox', () => {
         initialSearchType: 'messages',
         initialSearchTeam: 'teamId',
         crossTeamSearchEnabled: true,
+        myTeams: [{id: 'team1', name: 'team1', display_name: 'Team 1', description: ''}] as Team[],
     };
 
     test('should have the focus on the input field', () => {
@@ -72,4 +75,44 @@ describe('components/new_search/SearchBox', () => {
         expect(screen.getByText('Text file')).toHaveClass('selected');
         expect(screen.getByText('Word Document')).not.toHaveClass('selected');
     });
+
+    test('should show team selector when there is more than one team', () => {
+        const props = {
+            ...baseProps,
+            myTeams: [
+                {id: 'team1', name: 'team1', display_name: 'Team 1', description: ''} as Team,
+                {id: 'team2', name: 'team2', display_name: 'Team 2', description: ''} as Team,
+            ],
+        };
+        renderWithContext(<SearchBox {...props}/>);
+
+        // The select team dropdown should be visible
+        const teamSelector = document.querySelector('div[data-testid="searchTeamSelector"]');
+        expect(teamSelector).toBeInTheDocument();
+    });
+
+    test('should not show team selector when there is only one team', () => {
+        // Base props already has one team
+        renderWithContext(<SearchBox {...baseProps}/>);
+
+        // The select team dropdown should not be visible
+        const teamSelector = document.querySelector('div[data-testid="searchTeamSelector"]');
+        expect(teamSelector).not.toBeInTheDocument();
+    });
+
+    test('should not show team selector when cross-team search is disabled', () => {
+        const props = {
+            ...baseProps,
+            crossTeamSearchEnabled: false,
+            myTeams: [
+                {id: 'team1', name: 'team1', display_name: 'Team 1', description: ''} as Team,
+                {id: 'team2', name: 'team2', display_name: 'Team 2', description: ''} as Team,
+            ],
+        };
+        renderWithContext(<SearchBox {...props}/>);
+
+        // The select team dropdown should not be visible
+        const teamSelector = document.querySelector('div[data-testid="searchTeamSelector"]');
+        expect(teamSelector).not.toBeInTheDocument();
+    });
 });
diff --git a/webapp/channels/src/components/new_search/search_box.tsx b/webapp/channels/src/components/new_search/search_box.tsx
index aa0764a545..1b1cec64bb 100644
--- a/webapp/channels/src/components/new_search/search_box.tsx
+++ b/webapp/channels/src/components/new_search/search_box.tsx
@@ -5,6 +5,8 @@ import React, {useState, useRef, forwardRef, useCallback, useEffect} from 'react
 import {useIntl} from 'react-intl';
 import styled from 'styled-components';
 
+import type {Team} from '@mattermost/types/teams';
+
 import Constants from 'utils/constants';
 import * as Keyboard from 'utils/keyboard';
 import {escapeRegex} from 'utils/text_formatting';
@@ -25,6 +27,7 @@ type Props = {
     initialSearchType: string;
     initialSearchTeam: string;
     crossTeamSearchEnabled: boolean;
+    myTeams: Team[];
 };
 
 const SearchBoxContainer = styled.div`
@@ -73,7 +76,7 @@ const SearchTeamSelector = styled.div`
 
 const SearchBox = forwardRef(
     (
-        {onClose, onSearch, initialSearchTerms, initialSearchType, initialSearchTeam, crossTeamSearchEnabled}: Props,
+        {onClose, onSearch, initialSearchTerms, initialSearchType, initialSearchTeam, crossTeamSearchEnabled, myTeams}: Props,
         ref: React.Ref<HTMLDivElement>,
     ): JSX.Element => {
         const intl = useIntl();
@@ -83,6 +86,8 @@ const SearchBox = forwardRef(
         const [searchType, setSearchType] = useState<string>(initialSearchType || 'messages');
         const [selectedOption, setSelectedOption] = useState<number>(-1);
 
+        const hasMoreThanOneTeam = myTeams.length > 1;
+
         const inputRef = useRef<HTMLInputElement | null>(null);
 
         const [showFilterHaveBeenReset, setShowFilterHaveBeenReset] = useState(false);
@@ -282,8 +287,8 @@ const SearchBox = forwardRef(
                         searchType={searchType}
                         setSearchType={setSearchType}
                     />
-                    {crossTeamSearchEnabled && (
-                        <SearchTeamSelector>
+                    {crossTeamSearchEnabled && hasMoreThanOneTeam && (
+                        <SearchTeamSelector data-testid={'searchTeamSelector'}>
                             <SelectTeam
                                 selectedTeamId={searchTeam}
                                 onTeamSelected={changeSearchTeam}
diff --git a/webapp/channels/src/components/search_results/messages_or_files_selector.tsx b/webapp/channels/src/components/search_results/messages_or_files_selector.tsx
index 3c816aaeb7..ecddae40e7 100644
--- a/webapp/channels/src/components/search_results/messages_or_files_selector.tsx
+++ b/webapp/channels/src/components/search_results/messages_or_files_selector.tsx
@@ -5,6 +5,8 @@ import React, {useRef} from 'react';
 import {FormattedMessage} from 'react-intl';
 import {useSelector} from 'react-redux';
 
+import {getMyTeams} from 'mattermost-redux/selectors/entities/teams';
+
 import {getSearchTeam} from 'selectors/rhs';
 
 import SelectTeam from 'components/new_search/select_team';
@@ -39,6 +41,8 @@ type DataSearchLiteral = typeof DataSearchTypes[keyof typeof DataSearchTypes];
 
 export default function MessagesOrFilesSelector(props: Props): JSX.Element {
     const searchTeam = useSelector((state: GlobalState) => getSearchTeam(state));
+    const myTeams = useSelector(getMyTeams);
+    const hasMoreThanOneTeam = myTeams.length > 1;
 
     // REFS to the tabs so there is ability to pass the custom A11y focus event
     const messagesTabRef = useRef<HTMLButtonElement>(null);
@@ -130,7 +134,7 @@ export default function MessagesOrFilesSelector(props: Props): JSX.Element {
                     </button>
                 )}
             </div>
-            {props.crossTeamSearchEnabled && (
+            {props.crossTeamSearchEnabled && hasMoreThanOneTeam && (
                 <div className='team-selector-container'>
                     <SelectTeam
                         selectedTeamId={searchTeam}