diff --git a/crates/agent-gateway/web/src/app/GatewayApp.tsx b/crates/agent-gateway/web/src/app/GatewayApp.tsx
index 085f1633..1984dab8 100644
--- a/crates/agent-gateway/web/src/app/GatewayApp.tsx
+++ b/crates/agent-gateway/web/src/app/GatewayApp.tsx
@@ -207,6 +207,9 @@ export default function GatewayApp() {
   const { api, terminalClient, sftpClient, gitClient } = useGatewayClients(token);
   const [status, setStatus] = useState<AgentStatus | null>(null);
   const [statusError, setStatusError] = useState<string | null>(null);
+  // True only after an authenticated gateway connection has been established
+  // and then dropped; the initial connect (skeleton phase) never disables UI.
+  const [gatewayConnectionLost, setGatewayConnectionLost] = useState(false);
   const [conversationId, setConversationId] = useState("");
   const [chatError, setChatError] = useState<string | null>(null);
   // Sidebar errors raised outside the sidebar store (project removal flow).
@@ -1159,6 +1162,25 @@ export default function GatewayApp() {
     };
   }, [api]);
 
+  useEffect(() => {
+    if (!api) {
+      setGatewayConnectionLost(false);
+      return;
+    }
+    let wasConnected = false;
+    const unsubscribe = api.subscribeConnection((connected) => {
+      if (connected) {
+        wasConnected = true;
+        setGatewayConnectionLost(false);
+      } else if (wasConnected) {
+        setGatewayConnectionLost(true);
+      }
+    });
+    return () => {
+      unsubscribe();
+    };
+  }, [api]);
+
   const refreshChatQueueSnapshot = useCallback(
     (targetConversationId: string, currentApi = api) => {
       const conversationIdValue = targetConversationId.trim();
@@ -3579,6 +3601,7 @@ export default function GatewayApp() {
             canShareConversations={canShareHistory}
             sharedConversationCount={sharedHistoryItems.length}
             externalErrorMessage={sidebarActionError}
+            connectionLost={gatewayConnectionLost}
             isLocalDraftConversationId={isLocalDraftConversationId}
             onProjectsCollapsedChange={handleSidebarProjectsCollapsedChange}
             onRecentCollapsedChange={handleSidebarRecentCollapsedChange}
diff --git a/crates/agent-gateway/web/src/app/sidebar/GatewaySidebarContainer.tsx b/crates/agent-gateway/web/src/app/sidebar/GatewaySidebarContainer.tsx
index d28e7d32..64021d0b 100644
--- a/crates/agent-gateway/web/src/app/sidebar/GatewaySidebarContainer.tsx
+++ b/crates/agent-gateway/web/src/app/sidebar/GatewaySidebarContainer.tsx
@@ -32,6 +32,19 @@ function selectConversationIndex(snapshot: SidebarSnapshot) {
   return snapshot.byId;
 }
 
+// Transport-shaped list errors merely restate "the gateway socket is down";
+// the page-level banner owns that story, so the sidebar never repeats it —
+// including the stale copy that lingers until the reconnect refetch lands.
+// Mirrors isRecoverableGatewayTransportError in lib/gatewaySocket.ts.
+function isGatewayTransportErrorDetail(detail: string | null | undefined) {
+  const message = (detail ?? "").trim();
+  return (
+    message.startsWith("Gateway WebSocket disconnected") ||
+    message === "Gateway WebSocket is not connected" ||
+    message.startsWith("Gateway transport stalled")
+  );
+}
+
 // Stable identity wrapper so callback props from GatewayApp (recreated per
 // render) never churn effects or the memo'd view rows.
 function useStableCallback<Args extends unknown[], Return>(
@@ -63,6 +76,9 @@ export type GatewaySidebarContainerProps = {
   // GatewayApp-level sidebar errors (project removal flow); store errors are
   // derived locally and take precedence.
   externalErrorMessage: string | null;
+  // Gateway socket dropped after having been connected: the sections are
+  // disabled and error cards are suppressed (the page banner owns messaging).
+  connectionLost: boolean;
   isLocalDraftConversationId: (id: string) => boolean;
   onProjectsCollapsedChange: (collapsed: boolean) => void;
   onRecentCollapsedChange: (collapsed: boolean) => void;
@@ -92,7 +108,8 @@ export type GatewaySidebarContainerProps = {
 };
 
 export function GatewaySidebarContainer(props: GatewaySidebarContainerProps) {
-  const { store, projects, externalErrorMessage, isLocalDraftConversationId } = props;
+  const { store, projects, externalErrorMessage, connectionLost, isLocalDraftConversationId } =
+    props;
   const { t } = useLocale();
 
   const items = useSidebarSelector(store, selectConversations);
@@ -193,6 +210,9 @@ export function GatewaySidebarContainer(props: GatewaySidebarContainerProps) {
     [t],
   );
   const errorMessage = useMemo(() => {
+    if (connectionLost) {
+      return null;
+    }
     let lastMutationError: SidebarErrorCode | null = null;
     for (const code of mutationErrors.values()) {
       lastMutationError = code;
@@ -200,11 +220,12 @@ export function GatewaySidebarContainer(props: GatewaySidebarContainerProps) {
     if (lastMutationError) {
       return translateErrorCode(lastMutationError);
     }
-    if (listState.error) {
+    if (listState.error && !isGatewayTransportErrorDetail(listState.errorDetail)) {
       return listState.errorDetail?.trim() || translateErrorCode(listState.error);
     }
     return externalErrorMessage;
   }, [
+    connectionLost,
     externalErrorMessage,
     listState.error,
     listState.errorDetail,
@@ -234,6 +255,7 @@ export function GatewaySidebarContainer(props: GatewaySidebarContainerProps) {
       hasMore={listState.hasMore}
       isLoadingMore={listState.isLoadingMore}
       errorMessage={errorMessage}
+      sectionsDisabled={connectionLost}
       renamingId={renamingId}
       renameDraft={renameDraft}
       isOpen={props.isOpen}
diff --git a/crates/agent-gateway/web/src/components/chat/ChatHistorySidebar.tsx b/crates/agent-gateway/web/src/components/chat/ChatHistorySidebar.tsx
index fe1a7a32..8d6b4885 100644
--- a/crates/agent-gateway/web/src/components/chat/ChatHistorySidebar.tsx
+++ b/crates/agent-gateway/web/src/components/chat/ChatHistorySidebar.tsx
@@ -19,6 +19,7 @@ import {
 } from "../../lib/settings";
 import { cn } from "../../lib/shared/utils";
 import {
+  AlertCircle,
   ChevronRight,
   Edit3,
   Folder,
@@ -62,6 +63,9 @@ type ChatHistorySidebarProps = {
   hasMore: boolean;
   isLoadingMore: boolean;
   errorMessage: string | null;
+  // Disables the workspace + recent-conversation sections as one block (used
+  // while the gateway connection is lost); the header actions stay usable.
+  sectionsDisabled?: boolean;
   renamingId: string | null;
   renameDraft: string;
   isOpen: boolean;
@@ -1017,32 +1021,6 @@ function HistoryListLoadingSkeleton() {
   );
 }
 
-function SidebarStateCard(props: {
-  title: string;
-  description?: string;
-  tone?: "default" | "error";
-}) {
-  const { title, description, tone = "default" } = props;
-
-  return (
-    <div
-      className={cn(
-        "rounded-2xl border px-3 py-3 text-sm",
-        tone === "error"
-          ? "border-destructive/20 bg-destructive/5 text-destructive"
-          : "border-border/60 bg-background/70 text-muted-foreground",
-      )}
-    >
-      <div
-        className={cn("font-medium", tone === "error" ? "text-destructive" : "text-foreground/85")}
-      >
-        {title}
-      </div>
-      {description ? <div className="mt-1 text-xs leading-5">{description}</div> : null}
-    </div>
-  );
-}
-
 export const ChatHistorySidebar = memo(function ChatHistorySidebar(props: ChatHistorySidebarProps) {
   const {
     items,
@@ -1055,6 +1033,7 @@ export const ChatHistorySidebar = memo(function ChatHistorySidebar(props: ChatHi
     hasMore,
     isLoadingMore,
     errorMessage,
+    sectionsDisabled = false,
     renamingId,
     renameDraft,
     isOpen,
@@ -1655,9 +1634,12 @@ export const ChatHistorySidebar = memo(function ChatHistorySidebar(props: ChatHi
         <div
           ref={sidebarSectionsRef}
           style={{ gridTemplateRows: sidebarSectionLayout.gridTemplateRows }}
+          aria-disabled={sectionsDisabled || undefined}
+          inert={sectionsDisabled}
           className={cn(
             "grid min-h-0 flex-1 content-start",
             isProjectSectionResizing ? undefined : SIDEBAR_SECTION_ROWS_TRANSITION_CLASS,
+            sectionsDisabled && "pointer-events-none select-none opacity-50",
           )}
         >
           {showProjects ? (
@@ -1828,7 +1810,22 @@ export const ChatHistorySidebar = memo(function ChatHistorySidebar(props: ChatHi
                   {t("chat.history.syncing")}
                 </span>
               ) : null}
-              <div className="rounded-full border border-border/60 bg-background/80 px-2 py-0.5 text-[11px] font-medium text-muted-foreground">
+              <div
+                role={errorMessage ? "status" : undefined}
+                title={errorMessage ? `${t("chat.historyReadFailed")}: ${errorMessage}` : undefined}
+                className={cn(
+                  "flex items-center gap-1 rounded-full border px-2 py-0.5 text-[11px] font-medium",
+                  errorMessage
+                    ? "border-destructive/40 bg-destructive/10 text-destructive"
+                    : "border-border/60 bg-background/80 text-muted-foreground",
+                )}
+              >
+                {errorMessage ? (
+                  <AlertCircle
+                    className="h-3 w-3 shrink-0"
+                    aria-label={t("chat.historyReadFailed")}
+                  />
+                ) : null}
                 {Math.max(totalItems, items.length)}
               </div>
               {canShareConversations ? (
@@ -1863,19 +1860,10 @@ export const ChatHistorySidebar = memo(function ChatHistorySidebar(props: ChatHi
                 : "translate-y-0 opacity-100",
             )}
           >
-            {/* Render priority: error banner ABOVE rows (never replacing
-                them); skeleton only while loading with nothing cached; rows
-                whenever present; empty state only when authoritatively
-                empty. */}
-            {errorMessage ? (
-              <div className="shrink-0 px-3 pb-2">
-                <SidebarStateCard
-                  title={t("chat.historyReadFailed")}
-                  description={errorMessage}
-                  tone="error"
-                />
-              </div>
-            ) : null}
+            {/* Render priority: read failures surface as the red count badge
+                in the section header (never a card replacing rows); skeleton
+                only while loading with nothing cached; rows whenever present;
+                empty state only when authoritatively empty. */}
             <div
               ref={historyScrollRef}
               aria-busy={listStatus === "loading" || listStatus === "syncing" || isLoadingMore}
diff --git a/crates/agent-gateway/web/src/lib/sidebar/webSidebarBackend.ts b/crates/agent-gateway/web/src/lib/sidebar/webSidebarBackend.ts
index 44f46b57..38ae8c74 100644
--- a/crates/agent-gateway/web/src/lib/sidebar/webSidebarBackend.ts
+++ b/crates/agent-gateway/web/src/lib/sidebar/webSidebarBackend.ts
@@ -17,6 +17,7 @@
 import type { ActivityStore } from "@/lib/chat/stream/activityStore";
 import { formatConversationTitle } from "@/lib/chatUi";
 import type {
+  AgentStatus,
   ConversationSummary,
   GatewayHistoryEvent,
   HistoryList,
@@ -115,6 +116,7 @@ type WebSidebarApi = {
   deleteHistory(conversationId: string): Promise<void>;
   subscribeHistory(listener: (event: GatewayHistoryEvent) => void): () => void;
   subscribeConnection(listener: (connected: boolean) => void): () => void;
+  subscribeStatus(listener: (status: AgentStatus | null, error: string | null) => void): () => void;
 };
 
 export type WebSidebarBackendDeps = {
@@ -220,9 +222,38 @@ export function createWebSidebarBackend(deps: WebSidebarBackendDeps): SidebarBac
     },
 
     subscribeConnection(listener) {
-      // The client emits booleans already (true on auth, false on drop) and
-      // replays the current state to late subscribers.
-      return api.subscribeConnection((connected) => listener(connected === true));
+      // For the sidebar, "connected" means the whole read path works: the
+      // browser⇄gateway socket is authenticated AND the desktop agent behind
+      // it is online. The agent can drop and return while the socket never
+      // blips (and after a gateway restart the socket recovers before the
+      // agent has re-registered), so folding agent online-ness in here makes
+      // the store's reconnect refetch fire the moment reads can actually
+      // succeed — clearing any stale listError immediately instead of on the
+      // next reconcile tick. Both sources replay their current state to late
+      // subscribers; dedup keeps the store's disconnect latch edge-triggered.
+      let socketConnected = false;
+      let agentOnline = false;
+      let lastEmitted: boolean | null = null;
+      const emit = () => {
+        const next = socketConnected && agentOnline;
+        if (next === lastEmitted) {
+          return;
+        }
+        lastEmitted = next;
+        listener(next);
+      };
+      const unsubscribeConnection = api.subscribeConnection((connected) => {
+        socketConnected = connected === true;
+        emit();
+      });
+      const unsubscribeStatus = api.subscribeStatus((status) => {
+        agentOnline = status?.online === true;
+        emit();
+      });
+      return () => {
+        unsubscribeConnection();
+        unsubscribeStatus();
+      };
     },
 
     getProtectedConversationIds: () => deps.getProtectedConversationIds(),