diff --git a/res/css/views/rooms/_RoomSublist2.scss b/res/css/views/rooms/_RoomSublist2.scss
index ffb96cf600..43d1b3c7b3 100644
--- a/res/css/views/rooms/_RoomSublist2.scss
+++ b/res/css/views/rooms/_RoomSublist2.scss
@@ -278,6 +278,7 @@ limitations under the License.
     }
 
     &.mx_RoomSublist2_hasMenuOpen,
+    &:not(.mx_RoomSublist2_minimized) > .mx_RoomSublist2_headerContainer:focus-within,
     &:not(.mx_RoomSublist2_minimized) > .mx_RoomSublist2_headerContainer:hover {
         .mx_RoomSublist2_menuButton {
             visibility: visible;
diff --git a/res/css/views/rooms/_RoomTile2.scss b/res/css/views/rooms/_RoomTile2.scss
index ba8d315d5a..1fd32d3555 100644
--- a/res/css/views/rooms/_RoomTile2.scss
+++ b/res/css/views/rooms/_RoomTile2.scss
@@ -24,7 +24,10 @@ limitations under the License.
     // The tile is also a flexbox row itself
     display: flex;
 
-    &.mx_RoomTile2_selected, &:hover, &.mx_RoomTile2_hasMenuOpen {
+    &.mx_RoomTile2_selected,
+    &:hover,
+    &:focus-within,
+    &.mx_RoomTile2_hasMenuOpen {
         background-color: $roomtile2-selected-bg-color;
         border-radius: 32px;
     }
@@ -132,7 +135,9 @@ limitations under the License.
     }
 
     &:not(.mx_RoomTile2_minimized) {
-        &:hover, &.mx_RoomTile2_hasMenuOpen {
+        &:hover,
+        &:focus-within,
+        &.mx_RoomTile2_hasMenuOpen {
             // Hide the badge container on hover because it'll be a menu button
             .mx_RoomTile2_badgeContainer {
                 width: 0;
diff --git a/src/components/structures/LeftPanel2.tsx b/src/components/structures/LeftPanel2.tsx
index 83d5b9e138..0cf52039fe 100644
--- a/src/components/structures/LeftPanel2.tsx
+++ b/src/components/structures/LeftPanel2.tsx
@@ -30,7 +30,8 @@ import { BreadcrumbsStore } from "../../stores/BreadcrumbsStore";
 import { UPDATE_EVENT } from "../../stores/AsyncStore";
 import ResizeNotifier from "../../utils/ResizeNotifier";
 import SettingsStore from "../../settings/SettingsStore";
-import RoomListStore, { RoomListStore2, LISTS_UPDATE_EVENT } from "../../stores/room-list/RoomListStore2";
+import RoomListStore, { LISTS_UPDATE_EVENT } from "../../stores/room-list/RoomListStore2";
+import {Key} from "../../Keyboard";
 
 // TODO: Remove banner on launch: https://github.com/vector-im/riot-web/issues/14231
 // TODO: Rename on launch: https://github.com/vector-im/riot-web/issues/14231
@@ -57,6 +58,7 @@ interface IState {
 export default class LeftPanel2 extends React.Component<IProps, IState> {
     private listContainerRef: React.RefObject<HTMLDivElement> = createRef();
     private tagPanelWatcherRef: string;
+    private focusedElement = null;
 
     // TODO: a11y: https://github.com/vector-im/riot-web/issues/14180
 
@@ -150,6 +152,77 @@ export default class LeftPanel2 extends React.Component<IProps, IState> {
         this.handleStickyHeaders(this.listContainerRef.current);
     };
 
+    private onFocus = (ev: React.FocusEvent) => {
+        this.focusedElement = ev.target;
+    };
+
+    private onBlur = () => {
+        this.focusedElement = null;
+    };
+
+    private onKeyDown = (ev: React.KeyboardEvent) => {
+        if (!this.focusedElement) return;
+
+        switch (ev.key) {
+            case Key.ARROW_UP:
+            case Key.ARROW_DOWN:
+                this.onMoveFocus(ev, ev.key === Key.ARROW_UP);
+                break;
+        }
+    };
+
+    private onMoveFocus = (ev: React.KeyboardEvent, up: boolean) => {
+        let element = this.focusedElement;
+
+        // unclear why this isn't needed
+        // var descending = (up == this.focusDirection) ? this.focusDescending : !this.focusDescending;
+        // this.focusDirection = up;
+
+        let descending = false; // are we currently descending or ascending through the DOM tree?
+        let classes;
+
+        do {
+            const child = up ? element.lastElementChild : element.firstElementChild;
+            const sibling = up ? element.previousElementSibling : element.nextElementSibling;
+
+            if (descending) {
+                if (child) {
+                    element = child;
+                } else if (sibling) {
+                    element = sibling;
+                } else {
+                    descending = false;
+                    element = element.parentElement;
+                }
+            } else {
+                if (sibling) {
+                    element = sibling;
+                    descending = true;
+                } else {
+                    element = element.parentElement;
+                }
+            }
+
+            if (element) {
+                classes = element.classList;
+            }
+        } while (element && !(
+            classes.contains("mx_RoomTile2") ||
+            classes.contains("mx_RoomSublist2_headerText") ||
+            classes.contains("mx_RoomSearch_input")));
+
+        if (element) {
+            ev.stopPropagation();
+            ev.preventDefault();
+            element.focus();
+            this.focusedElement = element;
+        } else {
+            // if navigation is via up/down arrow-keys, trap in the widget so it doesn't send to composer
+            ev.stopPropagation();
+            ev.preventDefault();
+        }
+    };
+
     private renderHeader(): React.ReactNode {
         let breadcrumbs;
         if (this.state.showBreadcrumbs) {
@@ -170,8 +243,12 @@ export default class LeftPanel2 extends React.Component<IProps, IState> {
 
     private renderSearchExplore(): React.ReactNode {
         return (
-            <div className="mx_LeftPanel2_filterContainer">
-                <RoomSearch onQueryUpdate={this.onSearch} isMinimized={this.props.isMinimized} />
+            <div className="mx_LeftPanel2_filterContainer" onFocus={this.onFocus} onBlur={this.onBlur}>
+                <RoomSearch
+                    onQueryUpdate={this.onSearch}
+                    isMinimized={this.props.isMinimized}
+                    onVerticalArrow={this.onKeyDown}
+                />
                 <AccessibleButton
                     tabIndex={-1}
                     className='mx_LeftPanel2_exploreButton'
@@ -189,14 +266,13 @@ export default class LeftPanel2 extends React.Component<IProps, IState> {
             </div>
         );
 
-        // TODO: Determine what these onWhatever handlers do: https://github.com/vector-im/riot-web/issues/14180
         const roomList = <RoomList2
-            onKeyDown={() => {/*TODO*/}}
+            onKeyDown={this.onKeyDown}
             resizeNotifier={null}
             collapsed={false}
             searchFilter={this.state.searchFilter}
-            onFocus={() => {/*TODO*/}}
-            onBlur={() => {/*TODO*/}}
+            onFocus={this.onFocus}
+            onBlur={this.onBlur}
             isMinimized={this.props.isMinimized}
         />;
 
@@ -223,7 +299,12 @@ export default class LeftPanel2 extends React.Component<IProps, IState> {
                         className={roomListClasses}
                         onScroll={this.onScroll}
                         ref={this.listContainerRef}
-                    >{roomList}</div>
+                        // Firefox sometimes makes this element focusable due to
+                        // overflow:scroll;, so force it out of tab order.
+                        tabIndex={-1}
+                    >
+                        {roomList}
+                    </div>
                 </aside>
             </div>
         );
diff --git a/src/components/structures/RoomSearch.tsx b/src/components/structures/RoomSearch.tsx
index 8e64353954..7ed2acf276 100644
--- a/src/components/structures/RoomSearch.tsx
+++ b/src/components/structures/RoomSearch.tsx
@@ -38,6 +38,7 @@ import { Action } from "../../dispatcher/actions";
 interface IProps {
     onQueryUpdate: (newQuery: string) => void;
     isMinimized: boolean;
+    onVerticalArrow(ev: React.KeyboardEvent);
 }
 
 interface IState {
@@ -111,6 +112,8 @@ export default class RoomSearch extends React.PureComponent<IProps, IState> {
         if (ev.key === Key.ESCAPE) {
             this.clearInput();
             defaultDispatcher.fire(Action.FocusComposer);
+        } else if (ev.key === Key.ARROW_UP || ev.key === Key.ARROW_DOWN) {
+            this.props.onVerticalArrow(ev);
         }
     };
 
diff --git a/src/components/views/rooms/RoomSublist2.tsx b/src/components/views/rooms/RoomSublist2.tsx
index 547aa5e67e..c1f2a9ac79 100644
--- a/src/components/views/rooms/RoomSublist2.tsx
+++ b/src/components/views/rooms/RoomSublist2.tsx
@@ -35,6 +35,7 @@ import { DefaultTagID, TagID } from "../../../stores/room-list/models";
 import dis from "../../../dispatcher/dispatcher";
 import NotificationBadge from "./NotificationBadge";
 import { ListNotificationState } from "../../../stores/notifications/ListNotificationState";
+import { Key } from "../../../Keyboard";
 
 // TODO: Remove banner on launch: https://github.com/vector-im/riot-web/issues/14231
 // TODO: Rename on launch: https://github.com/vector-im/riot-web/issues/14231
@@ -80,6 +81,9 @@ interface IState {
 }
 
 export default class RoomSublist2 extends React.Component<IProps, IState> {
+    private headerButton = createRef<HTMLDivElement>();
+    private sublistRef = createRef<HTMLDivElement>();
+
     constructor(props: IProps) {
         super(props);
 
@@ -215,8 +219,52 @@ export default class RoomSublist2 extends React.Component<IProps, IState> {
             sublist.scrollIntoView({behavior: 'smooth'});
         } else {
             // on screen - toggle collapse
-            this.props.layout.isCollapsed = !this.props.layout.isCollapsed;
-            this.forceUpdate(); // because the layout doesn't trigger an update
+            this.toggleCollapsed();
+        }
+    };
+
+    private toggleCollapsed = () => {
+        this.props.layout.isCollapsed = !this.props.layout.isCollapsed;
+        this.forceUpdate(); // because the layout doesn't trigger an update
+    };
+
+    private onHeaderKeyDown = (ev: React.KeyboardEvent) => {
+        const isCollapsed = this.props.layout && this.props.layout.isCollapsed;
+        switch (ev.key) {
+            case Key.ARROW_LEFT:
+                ev.stopPropagation();
+                if (!isCollapsed) {
+                    // On ARROW_LEFT collapse the room sublist if it isn't already
+                    this.toggleCollapsed();
+                }
+                break;
+            case Key.ARROW_RIGHT: {
+                ev.stopPropagation();
+                if (isCollapsed) {
+                    // On ARROW_RIGHT expand the room sublist if it isn't already
+                    this.toggleCollapsed();
+                } else if (this.sublistRef.current) {
+                    // otherwise focus the first room
+                    const element = this.sublistRef.current.querySelector(".mx_RoomTile2") as HTMLDivElement;
+                    if (element) {
+                        element.focus();
+                    }
+                }
+                break;
+            }
+        }
+    };
+
+    private onKeyDown = (ev: React.KeyboardEvent) => {
+        switch (ev.key) {
+            // On ARROW_LEFT go to the sublist header
+            case Key.ARROW_LEFT:
+                ev.stopPropagation();
+                this.headerButton.current.focus();
+                break;
+            // Consume ARROW_RIGHT so it doesn't cause focus to get sent to composer
+            case Key.ARROW_RIGHT:
+                ev.stopPropagation();
         }
     };
 
@@ -335,7 +383,6 @@ export default class RoomSublist2 extends React.Component<IProps, IState> {
         return (
             <RovingTabIndexWrapper>
                 {({onFocus, isActive, ref}) => {
-                    // TODO: Use onFocus: https://github.com/vector-im/riot-web/issues/14180
                     const tabIndex = isActive ? 0 : -1;
 
                     const badge = (
@@ -382,13 +429,13 @@ export default class RoomSublist2 extends React.Component<IProps, IState> {
                     // doesn't become sticky.
                     // The same applies to the notification badge.
                     return (
-                        <div className={classes}>
-                            <div className='mx_RoomSublist2_stickable'>
+                        <div className={classes} onKeyDown={this.onHeaderKeyDown} onFocus={onFocus}>
+                            <div className="mx_RoomSublist2_stickable">
                                 <AccessibleButton
                                     onFocus={onFocus}
                                     inputRef={ref}
                                     tabIndex={tabIndex}
-                                    className={"mx_RoomSublist2_headerText"}
+                                    className="mx_RoomSublist2_headerText"
                                     role="treeitem"
                                     aria-level={1}
                                     onClick={this.onHeaderClick}
@@ -516,12 +563,13 @@ export default class RoomSublist2 extends React.Component<IProps, IState> {
             );
         }
 
-        // TODO: onKeyDown support: https://github.com/vector-im/riot-web/issues/14180
         return (
             <div
+                ref={this.sublistRef}
                 className={classes}
                 role="group"
                 aria-label={this.props.label}
+                onKeyDown={this.onKeyDown}
             >
                 {this.renderHeader()}
                 {content}
diff --git a/src/components/views/rooms/RoomTile2.tsx b/src/components/views/rooms/RoomTile2.tsx
index 92c69e54e7..a85ebe7dd3 100644
--- a/src/components/views/rooms/RoomTile2.tsx
+++ b/src/components/views/rooms/RoomTile2.tsx
@@ -235,7 +235,7 @@ export default class RoomTile2 extends React.Component<IProps, IState> {
     private onClickMentions = ev => this.saveNotifState(ev, MENTIONS_ONLY);
     private onClickMute = ev => this.saveNotifState(ev, MUTE);
 
-    private renderNotificationsMenu(): React.ReactElement {
+    private renderNotificationsMenu(isActive: boolean): React.ReactElement {
         if (this.props.isMinimized || MatrixClientPeg.get().isGuest() || this.props.tag === DefaultTagID.Invite) {
             // the menu makes no sense in these cases so do not show one
             return null;
@@ -296,6 +296,7 @@ export default class RoomTile2 extends React.Component<IProps, IState> {
                     onClick={this.onNotificationsMenuOpenClick}
                     label={_t("Notification options")}
                     isExpanded={!!this.state.notificationsMenuPosition}
+                    tabIndex={isActive ? 0 : -1}
                 />
                 {contextMenu}
             </React.Fragment>
@@ -434,7 +435,7 @@ export default class RoomTile2 extends React.Component<IProps, IState> {
                             {roomAvatar}
                             {nameContainer}
                             {badge}
-                            {this.renderNotificationsMenu()}
+                            {this.renderNotificationsMenu(isActive)}
                             {this.renderGeneralMenu()}
                         </AccessibleButton>
                     }