diff --git a/web/packages/teleterm/src/ui/TopBar/Clusters/ClustersFilterableList/ClusterItem.tsx b/web/packages/teleterm/src/ui/TopBar/Clusters/ClustersFilterableList/ClusterItem.tsx
index 622f1ccc76fc3..faef48a3a9c68 100644
--- a/web/packages/teleterm/src/ui/TopBar/Clusters/ClustersFilterableList/ClusterItem.tsx
+++ b/web/packages/teleterm/src/ui/TopBar/Clusters/ClustersFilterableList/ClusterItem.tsx
@@ -16,7 +16,7 @@
  * along with this program.  If not, see <http://www.gnu.org/licenses/>.
  */
 
-import React from 'react';
+import { useRef, useEffect } from 'react';
 import { Flex, Label, Text } from 'design';
 
 import styled from 'styled-components';
@@ -33,15 +33,21 @@ interface ClusterItemProps {
 }
 
 export function ClusterItem(props: ClusterItemProps) {
-  const { isActive } = useKeyboardArrowsNavigation({
+  const { isActive, scrollIntoViewIfActive } = useKeyboardArrowsNavigation({
     index: props.index,
     onRun: props.onSelect,
   });
+  const ref = useRef<HTMLElement>();
 
   const clusterName = props.item.name;
 
+  useEffect(() => {
+    scrollIntoViewIfActive(ref.current);
+  }, [scrollIntoViewIfActive]);
+
   return (
     <StyledListItem
+      ref={ref}
       onClick={props.onSelect}
       isActive={isActive}
       isSelected={props.isSelected}
diff --git a/web/packages/teleterm/src/ui/TopBar/Connections/Connections.story.tsx b/web/packages/teleterm/src/ui/TopBar/Connections/Connections.story.tsx
index 127023e682579..f28b505e6cea3 100644
--- a/web/packages/teleterm/src/ui/TopBar/Connections/Connections.story.tsx
+++ b/web/packages/teleterm/src/ui/TopBar/Connections/Connections.story.tsx
@@ -17,6 +17,7 @@
  */
 
 import { useLayoutEffect } from 'react';
+import { Flex, Text } from 'design';
 
 import AppContextProvider from 'teleterm/ui/appContextProvider';
 import { MockAppContext } from 'teleterm/ui/fixtures/mocks';
@@ -62,6 +63,48 @@ export function JustVnet() {
   );
 }
 
+export function WithScroll() {
+  const appContext = new MockAppContext();
+  prepareAppContext(appContext);
+  appContext.connectionTracker.getConnections = () => [
+    {
+      connected: false,
+      kind: 'connection.server' as const,
+      title: 'last-item',
+      id: 'last-item',
+      serverUri: '/clusters/foo/servers/last-item',
+      login: 'item',
+      clusterName: 'teleport.example.sh',
+    },
+    ...Array(10)
+      .fill(undefined)
+      .flatMap((_, index) => makeConnections(index)),
+  ];
+
+  return (
+    <Flex
+      flexDirection="row"
+      justifyContent="space-between"
+      gap={3}
+      minWidth="500px"
+      maxWidth="600px"
+    >
+      <AppContextProvider value={appContext}>
+        <VnetContextProvider>
+          <Connections />
+        </VnetContextProvider>
+      </AppContextProvider>
+      <Text
+        css={`
+          max-width: 20ch;
+        `}
+      >
+        Manipulate window height to simulate how the list behaves in Connect.
+      </Text>
+    </Flex>
+  );
+}
+
 export function WithoutVnet() {
   const appContext = new MockAppContext({ platform: 'win32' });
   prepareAppContext(appContext);
@@ -87,40 +130,44 @@ export function EmptyWithoutVnet() {
   );
 }
 
+const makeConnections = (index = 0) => {
+  const suffix = index === 0 ? '' : `-${index}`;
+
+  return [
+    {
+      connected: true,
+      kind: 'connection.server' as const,
+      title: 'ansible' + suffix,
+      id: 'e9c4fbc2' + suffix,
+      serverUri: '/clusters/foo/servers/ansible' + suffix,
+      login: 'casey',
+      clusterName: 'teleport.example.sh',
+    },
+    {
+      connected: true,
+      kind: 'connection.gateway' as const,
+      title: 'postgres' + suffix,
+      targetName: 'postgres',
+      id: '68b6a281' + suffix,
+      targetUri: '/clusters/foo/dbs/brock' + suffix,
+      port: '22',
+      gatewayUri: '/gateways/empty',
+      clusterName: 'teleport.example.sh',
+    },
+    {
+      connected: false,
+      kind: 'connection.server' as const,
+      title: 'ansible-staging' + suffix,
+      id: '949651ed' + suffix,
+      serverUri: '/clusters/foo/servers/ansible-staging' + suffix,
+      login: 'casey',
+      clusterName: 'teleport.example.sh',
+    },
+  ];
+};
+
 const prepareAppContext = (appContext: MockAppContext) => {
-  appContext.connectionTracker.getConnections = () => {
-    return [
-      {
-        connected: true,
-        kind: 'connection.server',
-        title: 'ansible',
-        id: 'e9c4fbc2',
-        serverUri: '/clusters/foo/servers/ansible',
-        login: 'casey',
-        clusterName: 'teleport.example.sh',
-      },
-      {
-        connected: true,
-        kind: 'connection.gateway',
-        title: 'postgres',
-        targetName: 'postgres',
-        id: '68b6a281',
-        targetUri: '/clusters/foo/dbs/brock',
-        port: '22',
-        gatewayUri: '/gateways/empty',
-        clusterName: 'teleport.example.sh',
-      },
-      {
-        connected: false,
-        kind: 'connection.server',
-        title: 'ansible-staging',
-        id: '949651ed',
-        serverUri: '/clusters/foo/servers/ansible-staging',
-        login: 'casey',
-        clusterName: 'teleport.example.sh',
-      },
-    ];
-  };
+  appContext.connectionTracker.getConnections = () => makeConnections();
   appContext.connectionTracker.activateItem = async () => {};
   appContext.connectionTracker.disconnectItem = async () => {};
   appContext.connectionTracker.removeItem = async () => {};
@@ -130,6 +177,14 @@ const prepareAppContext = (appContext: MockAppContext) => {
 
 const useOpenConnections = () => {
   useLayoutEffect(() => {
+    const areConnectionsOpen = !!document.querySelector(
+      'input[role=searchbox]'
+    );
+
+    if (areConnectionsOpen) {
+      return;
+    }
+
     const button = document.querySelector(
       'button[title~="connections"i]'
     ) as HTMLButtonElement;
diff --git a/web/packages/teleterm/src/ui/TopBar/Connections/ConnectionsFilterableList/ConnectionItem.tsx b/web/packages/teleterm/src/ui/TopBar/Connections/ConnectionsFilterableList/ConnectionItem.tsx
index 8e259de97d9f0..d01130c0007ea 100644
--- a/web/packages/teleterm/src/ui/TopBar/Connections/ConnectionsFilterableList/ConnectionItem.tsx
+++ b/web/packages/teleterm/src/ui/TopBar/Connections/ConnectionsFilterableList/ConnectionItem.tsx
@@ -16,7 +16,7 @@
  * along with this program.  If not, see <http://www.gnu.org/licenses/>.
  */
 
-import React from 'react';
+import { useEffect, useRef } from 'react';
 import { ButtonIcon, Flex, Text } from 'design';
 import { Trash, Unlink } from 'design/Icon';
 
@@ -41,7 +41,7 @@ interface ConnectionItemProps {
 
 export function ConnectionItem(props: ConnectionItemProps) {
   const offline = !props.item.connected;
-  const { isActive } = useKeyboardArrowsNavigation({
+  const { isActive, scrollIntoViewIfActive } = useKeyboardArrowsNavigation({
     index: props.index,
     onRun: props.onActivate,
   });
@@ -60,11 +60,17 @@ export function ConnectionItem(props: ConnectionItemProps) {
   };
 
   const actionIcon = offline ? actionIcons.remove : actionIcons.disconnect;
+  const ref = useRef<HTMLElement>();
+
+  useEffect(() => {
+    scrollIntoViewIfActive(ref.current);
+  }, [scrollIntoViewIfActive]);
 
   return (
     <ListItem
       onClick={props.onActivate}
       isActive={isActive}
+      ref={ref}
       css={`
         padding: 6px 8px;
         height: unset;
diff --git a/web/packages/teleterm/src/ui/components/FilterableList/FilterableList.test.tsx b/web/packages/teleterm/src/ui/components/FilterableList/FilterableList.test.tsx
index 132880876d0c7..68dca2a049afb 100644
--- a/web/packages/teleterm/src/ui/components/FilterableList/FilterableList.test.tsx
+++ b/web/packages/teleterm/src/ui/components/FilterableList/FilterableList.test.tsx
@@ -34,7 +34,7 @@ function Node({ item }: { item: TestItem }) {
   return <li>{item.title}</li>;
 }
 
-test('render first 10 items by default', () => {
+test('render all items by default', () => {
   render(
     <FilterableList<TestItem>
       items={mockedItems}
@@ -44,7 +44,7 @@ test('render first 10 items by default', () => {
   );
   const items = screen.getAllByRole('listitem');
 
-  expect(items).toHaveLength(10);
+  expect(items).toHaveLength(30);
   items.forEach((item, index) => {
     expect(item).toHaveTextContent(mockedItems[index].title);
   });
diff --git a/web/packages/teleterm/src/ui/components/FilterableList/FilterableList.tsx b/web/packages/teleterm/src/ui/components/FilterableList/FilterableList.tsx
index e4ea227eec265..a58bf70930eb1 100644
--- a/web/packages/teleterm/src/ui/components/FilterableList/FilterableList.tsx
+++ b/web/packages/teleterm/src/ui/components/FilterableList/FilterableList.tsx
@@ -30,8 +30,6 @@ interface FilterableListProps<T> {
   onFilterChange?(filter: string): void;
 }
 
-const maxItemsToShow = 10;
-
 export function FilterableList<T>(
   props: React.PropsWithChildren<FilterableListProps<T>>
 ) {
@@ -39,8 +37,7 @@ export function FilterableList<T>(
   const [searchValue, setSearchValue] = useState<string>();
 
   const filteredItems = useMemo(
-    () =>
-      filterItems(searchValue, items, props.filterBy).slice(0, maxItemsToShow),
+    () => filterItems(searchValue, items, props.filterBy),
     [items, searchValue]
   );
 
@@ -84,7 +81,7 @@ const UnorderedList = styled.ul`
 `;
 
 const StyledInput = styled(Input)`
-  background: inherit;
+  background-color: inherit;
   border-radius: 51px;
   margin-bottom: 8px;
   font-size: 14px;
diff --git a/web/packages/teleterm/src/ui/components/KeyboardArrowsNavigation/useKeyboardArrowsNavigation.ts b/web/packages/teleterm/src/ui/components/KeyboardArrowsNavigation/useKeyboardArrowsNavigation.ts
index 7847e386f3221..c37e67482d5c4 100644
--- a/web/packages/teleterm/src/ui/components/KeyboardArrowsNavigation/useKeyboardArrowsNavigation.ts
+++ b/web/packages/teleterm/src/ui/components/KeyboardArrowsNavigation/useKeyboardArrowsNavigation.ts
@@ -16,7 +16,7 @@
  * along with this program.  If not, see <http://www.gnu.org/licenses/>.
  */
 
-import { useContext, useEffect } from 'react';
+import { useCallback, useContext, useEffect } from 'react';
 
 import {
   KeyboardArrowsNavigationContext,
@@ -48,8 +48,35 @@ export function useKeyboardArrowsNavigation({
     return () => navigationContext.removeItem(index);
   }, [index, onRun, navigationContext.addItem, navigationContext.removeItem]);
 
+  const isActive = index === navigationContext.activeIndex;
+
+  const scrollIntoViewIfActive = useCallback(
+    (el: HTMLElement | undefined) => {
+      if (!isActive || !el) {
+        return;
+      }
+
+      // By default, scrollIntoView uses 'start'. This is a problem in two cases:
+      //
+      // 1. When scrolling from the last to the first element, the top of the scrollable area gets
+      // aligned to the top of the first active element, not to the top of the parent container.
+      // 2. When scrolling from any other element to the next one, the scrollable area gets aligned
+      // to the top of the active element, meaning that the previous element immediately disappears.
+      //
+      // 'center' fixes both problems, while being closer than 'nearest' to how the browser adjusts
+      // the scrollable area when tabbing through focusable elements. It ensures that you see what's
+      // after and before the active element.
+      //
+      // Compared to 'nearest', it also makes sure that the scrollable area is aligned to its bottom
+      // when scrolling to the last element – 'nearest' aligns it to the bottom of the active item.
+      el.scrollIntoView({ block: 'center' });
+    },
+    [isActive]
+  );
+
   return {
-    isActive: index === navigationContext.activeIndex,
+    isActive,
+    scrollIntoViewIfActive,
   };
 }