diff --git a/libs/i18n/locales/en/translation.json b/libs/i18n/locales/en/translation.json
index e6b0ee214..9b6cccaf4 100644
--- a/libs/i18n/locales/en/translation.json
+++ b/libs/i18n/locales/en/translation.json
@@ -608,13 +608,11 @@
   "Restarts": "Restarts",
   "Workload applications": "Workload applications",
   "Virtual machines": "Virtual machines",
+  "The application has restarted {{ restartDelta }} times this session and may be misconfigured. Stop the application to prevent further restarts and investigate the issue.": "The application has restarted {{ restartDelta }} times this session and may be misconfigured. Stop the application to prevent further restarts and investigate the issue.",
+  "The application has restarted {{ restartDelta }} times this session and may be misconfigured. Contact an administrator to stop the application and investigate the issue.": "The application has restarted {{ restartDelta }} times this session and may be misconfigured. Contact an administrator to stop the application and investigate the issue.",
   "Stop application": "Stop application",
   "Restart loop detected": "Restart loop detected",
-  "This application has restarted {{ count }} times this session. Stop the application to prevent further restarts and investigate the issue._one": "This application has restarted {{ count }} times this session. Stop the application to prevent further restarts and investigate the issue.",
-  "This application has restarted {{ count }} times this session. Stop the application to prevent further restarts and investigate the issue._other": "This application has restarted {{ count }} times this session. Stop the application to prevent further restarts and investigate the issue.",
   "This application is restarting repeatedly": "This application is restarting repeatedly",
-  "The application has restarted {{ count }} times this session and may be misconfigured. Stop the application to prevent further restarts and investigate the issue._one": "The application has restarted {{ count }} times this session and may be misconfigured. Stop the application to prevent further restarts and investigate the issue.",
-  "The application has restarted {{ count }} times this session and may be misconfigured. Stop the application to prevent further restarts and investigate the issue._other": "The application has restarted {{ count }} times this session and may be misconfigured. Stop the application to prevent further restarts and investigate the issue.",
   "No applications found": "No applications found",
   "Applications": "Applications",
   "Message": "Message",
@@ -1871,8 +1869,10 @@
   "{{ numberOfItems }} items": "{{ numberOfItems }} items",
   "Search value cannot contain spaces": "Search value cannot contain spaces",
   "The virtual machine is starting. Console will be available once running.": "The virtual machine is starting. Console will be available once running.",
+  "The virtual machine is stopped. Start the VM to access the console.": "The virtual machine is stopped. Start the VM to access the console.",
+  "The virtual machine is stopping. Start the VM to access the console.": "The virtual machine is stopping. Start the VM to access the console.",
   "The virtual machine is not running. Start the VM to access the console.": "The virtual machine is not running. Start the VM to access the console.",
-  "Connection was closed": "Connection was closed",
+  "Connection was closed. The VM may be starting, stopping, or stopped.": "Connection was closed. The VM may be starting, stopping, or stopped.",
   "Reconnect": "Reconnect",
   "Connected to serial console: {{ appName }}": "Connected to serial console: {{ appName }}",
   "No virtual machines found. Create a virtual machine to access its serial console.": "No virtual machines found. Create a virtual machine to access its serial console.",
@@ -1884,9 +1884,11 @@
   "End active console session?": "End active console session?",
   "This will terminate the existing console session for \"{{appName}}\". If another user is connected, they will be disconnected immediately.": "This will terminate the existing console session for \"{{appName}}\". If another user is connected, they will be disconnected immediately.",
   "End session and connect": "End session and connect",
+  "Connection was closed": "Connection was closed",
   "Waiting for terminal session to open...": "Waiting for terminal session to open...",
   "Only one serial console session can be active at a time. Another user or browser tab may already be connected to this virtual machine. Close any other active session, then try again.": "Only one serial console session can be active at a time. Another user or browser tab may already be connected to this virtual machine. Close any other active session, then try again.",
   "This console session was ended because another user connected to the same virtual machine.": "This console session was ended because another user connected to the same virtual machine.",
+  "The virtual machine console is unavailable at the moment. The VM may be starting, stopping, or stopped.": "The virtual machine console is unavailable at the moment. The VM may be starting, stopping, or stopped.",
   "You do not have permission to access the virtual machine console.": "You do not have permission to access the virtual machine console.",
   "The virtual machine application was not found.": "The virtual machine application was not found.",
   "Timed out connecting to the virtual machine console. The VM may still be starting.": "Timed out connecting to the virtual machine console. The VM may still be starting.",
diff --git a/libs/ui-components/src/components/DetailsPage/Tables/ApplicationLifecycleActions.tsx b/libs/ui-components/src/components/DetailsPage/Tables/ApplicationLifecycleActions.tsx
index 00abd875a..1b793430b 100644
--- a/libs/ui-components/src/components/DetailsPage/Tables/ApplicationLifecycleActions.tsx
+++ b/libs/ui-components/src/components/DetailsPage/Tables/ApplicationLifecycleActions.tsx
@@ -19,6 +19,7 @@ import { getDisabledTooltipProps } from '../../../utils/tooltip';
 import {
   type ApplicationLifecycleAction,
   hasAplicationStatusMismatch,
+  isAppConsoleAvailable,
   startableStatuses,
   stoppableStatuses,
   transitionalStatuses,
@@ -108,6 +109,7 @@ const ApplicationLifecycleActions = ({
 
   const isAppRunning = appStatus === ApplicationStatusType.ApplicationStatusRunning;
   const desiredStateIsStopped = desiredState === ApplicationDesiredState.ApplicationDesiredStateStopped;
+  const canOpenConsole = isAppConsoleAvailable(appStatus, desiredState);
   const canStart = startableStatuses.includes(appStatus);
   const canStop = stoppableStatuses.includes(appStatus);
   const isTransitioning = transitionalStatuses.includes(appStatus);
@@ -192,7 +194,7 @@ const ApplicationLifecycleActions = ({
                 <Button
                   variant={ButtonVariant.link}
                   icon={<TerminalIcon />}
-                  isDisabled={!isAppRunning}
+                  isDisabled={!canOpenConsole}
                   onClick={() => onOpenConsole?.(appStatusObj.name)}
                 >
                   {t('Open console')}
diff --git a/libs/ui-components/src/components/DetailsPage/Tables/ApplicationsTable.tsx b/libs/ui-components/src/components/DetailsPage/Tables/ApplicationsTable.tsx
index ceb0a054a..a3bd974de 100644
--- a/libs/ui-components/src/components/DetailsPage/Tables/ApplicationsTable.tsx
+++ b/libs/ui-components/src/components/DetailsPage/Tables/ApplicationsTable.tsx
@@ -89,27 +89,49 @@ const AppExpandedDetails = ({
   return <WorkloadAppExpandedDetails application={application} desiredState={desiredState} />;
 };
 
-type RestartLoopStopButtonProps = {
-  onStop: () => void;
-  isDisabled: boolean;
-  isLoading: boolean;
-};
-
-const RestartLoopStopButton = ({ onStop, isDisabled, isLoading }: RestartLoopStopButtonProps) => {
-  const { t } = useTranslation();
-  return (
-    <Button variant="secondary" onClick={onStop} isDisabled={isDisabled} isLoading={isLoading}>
-      {t('Stop application')}
-    </Button>
-  );
-};
-
 type RestartLoopWarningProps = {
   restartDelta: number;
   canStop: boolean;
   stopDisabled: boolean;
   stopLoading: boolean;
-  onStop: () => void;
+  onStop: VoidFunction;
+};
+
+const RestartLoopWarningContent = ({
+  restartDelta,
+  canStop,
+  stopDisabled,
+  stopLoading,
+  onStop,
+}: RestartLoopWarningProps) => {
+  const { t } = useTranslation();
+  return (
+    <Stack hasGutter>
+      <StackItem>
+        {canStop
+          ? t(
+              'The application has restarted {{ restartDelta }} times this session and may be misconfigured. Stop the application to prevent further restarts and investigate the issue.',
+              { restartDelta },
+            )
+          : t(
+              'The application has restarted {{ restartDelta }} times this session and may be misconfigured. Contact an administrator to stop the application and investigate the issue.',
+              { restartDelta },
+            )}
+      </StackItem>
+      {canStop && (
+        <Button
+          variant="secondary"
+          size="sm"
+          onClick={onStop}
+          isDisabled={stopDisabled}
+          isLoading={stopLoading}
+          style={{ width: 'fit-content' }}
+        >
+          {t('Stop application')}
+        </Button>
+      )}
+    </Stack>
+  );
 };
 
 const AppRestartsWarning = ({
@@ -121,31 +143,23 @@ const AppRestartsWarning = ({
   onStop,
 }: RestartLoopWarningProps & { restarts: number }) => {
   const { t } = useTranslation();
+  const warningTitle = t('Restart loop detected');
   return (
     <Popover
-      aria-label={t('Restart loop detected')}
-      headerContent={t('Restart loop detected')}
+      aria-label={warningTitle}
+      headerContent={warningTitle}
       bodyContent={
-        <Stack hasGutter>
-          <StackItem>
-            {t(
-              'This application has restarted {{ count }} times this session. Stop the application to prevent further restarts and investigate the issue.',
-              {
-                count: restartDelta,
-              },
-            )}
-          </StackItem>
-
-          {canStop && (
-            <StackItem>
-              <RestartLoopStopButton onStop={onStop} isDisabled={stopDisabled} isLoading={stopLoading} />
-            </StackItem>
-          )}
-        </Stack>
+        <RestartLoopWarningContent
+          restartDelta={restartDelta}
+          canStop={canStop}
+          stopDisabled={stopDisabled}
+          stopLoading={stopLoading}
+          onStop={onStop}
+        />
       }
       withFocusTrap={false}
     >
-      <Button aria-label={t('Restart loop detected')} variant="link" isInline>
+      <Button aria-label={warningTitle} variant="link" isInline>
         <Label status="warning" variant="outline">
           {restarts}
         </Label>
@@ -154,29 +168,6 @@ const AppRestartsWarning = ({
   );
 };
 
-const RestartLoopAlert = ({ restartDelta, canStop, stopDisabled, stopLoading, onStop }: RestartLoopWarningProps) => {
-  const { t } = useTranslation();
-  return (
-    <Alert isInline variant="warning" title={t('This application is restarting repeatedly')}>
-      <Stack hasGutter>
-        <StackItem>
-          {t(
-            'The application has restarted {{ count }} times this session and may be misconfigured. Stop the application to prevent further restarts and investigate the issue.',
-            {
-              count: restartDelta,
-            },
-          )}
-        </StackItem>
-        {canStop && (
-          <StackItem>
-            <RestartLoopStopButton onStop={onStop} isDisabled={stopDisabled} isLoading={stopLoading} />
-          </StackItem>
-        )}
-      </Stack>
-    </Alert>
-  );
-};
-
 type ApplicationTableRowProps = BaseApplicationsTableProps & {
   desiredState?: ApplicationDesiredState;
   application: StatusAppWithSpec;
@@ -284,13 +275,15 @@ const ApplicationTableRow = ({
               </StackItem>
               {showRestartLoopWarning && isExpanded && (
                 <StackItem>
-                  <RestartLoopAlert
-                    restartDelta={restartDelta}
-                    canStop={canStop}
-                    stopDisabled={isStopDisabled}
-                    stopLoading={lifecycle.isSubmitting}
-                    onStop={onStop}
-                  />
+                  <Alert isInline variant="warning" title={t('This application is restarting repeatedly')}>
+                    <RestartLoopWarningContent
+                      restartDelta={restartDelta}
+                      canStop={canStop}
+                      stopDisabled={isStopDisabled}
+                      stopLoading={lifecycle.isSubmitting}
+                      onStop={onStop}
+                    />
+                  </Alert>
                 </StackItem>
               )}
               <StackItem>
diff --git a/libs/ui-components/src/components/Terminal/AppTerminal.tsx b/libs/ui-components/src/components/Terminal/AppTerminal.tsx
index e063a5a95..7f234807d 100644
--- a/libs/ui-components/src/components/Terminal/AppTerminal.tsx
+++ b/libs/ui-components/src/components/Terminal/AppTerminal.tsx
@@ -1,4 +1,5 @@
 import * as React from 'react';
+import type { TFunction } from 'react-i18next';
 import {
   Alert,
   AlertActionLink,
@@ -13,14 +14,43 @@ import {
   StackItem,
 } from '@patternfly/react-core';
 
-import { ApplicationStatusType, type Device, type DeviceApplicationStatus } from '@flightctl/types';
+import {
+  ApplicationDesiredState,
+  ApplicationStatusType,
+  type Device,
+  type DeviceApplicationStatus,
+} from '@flightctl/types';
 
 import { useTranslation } from '../../hooks/useTranslation';
 import { type AppConsoleConnectError, useAppConsoleWebSocket } from '../../hooks/useAppConsoleWebSocket';
+import { getDeviceAppLifecycleOverrides, isAppConsoleAvailable } from '../../utils/applicationLifecycle';
 import { useOrganizationGuardContext } from '../common/OrganizationGuard';
 import TerminalConnectError from './TerminalConnectError';
 import Terminal, { type ImperativeTerminalType } from './Terminal';
 
+const getAppTerminalUnavailableTitle = (
+  t: TFunction,
+  status: ApplicationStatusType,
+  desiredState: ApplicationDesiredState | undefined,
+) => {
+  switch (status) {
+    case ApplicationStatusType.ApplicationStatusStarting:
+    case ApplicationStatusType.ApplicationStatusPreparing:
+      return t('The virtual machine is starting. Console will be available once running.');
+    case ApplicationStatusType.ApplicationStatusStopped:
+    case ApplicationStatusType.ApplicationStatusCompleted:
+      return t('The virtual machine is stopped. Start the VM to access the console.');
+    case ApplicationStatusType.ApplicationStatusStopping:
+      return t('The virtual machine is stopping. Start the VM to access the console.');
+    default:
+      if (desiredState === ApplicationDesiredState.ApplicationDesiredStateStopped) {
+        // App is currently running, but it has been signaled to stop.
+        return t('The virtual machine is stopping. Start the VM to access the console.');
+      }
+      return t('The virtual machine is not running. Start the VM to access the console.');
+  }
+};
+
 const AppTerminalContent = ({
   appStatus,
   sendMessage,
@@ -48,23 +78,6 @@ const AppTerminalContent = ({
     [terminalRef, reconnect],
   );
 
-  if (appStatus.status !== ApplicationStatusType.ApplicationStatusRunning) {
-    return (
-      <Bullseye>
-        <Alert
-          variant="info"
-          isInline
-          isPlain
-          title={
-            appStatus.status === ApplicationStatusType.ApplicationStatusStarting
-              ? t('The virtual machine is starting. Console will be available once running.')
-              : t('The virtual machine is not running. Start the VM to access the console.')
-          }
-        />
-      </Bullseye>
-    );
-  }
-
   if (isConnecting) {
     return (
       <Bullseye data-testid="app-console-loading">
@@ -90,7 +103,7 @@ const AppTerminalContent = ({
         <Alert
           isInline
           variant="info"
-          title={t('Connection was closed')}
+          title={t('Connection was closed. The VM may be starting, stopping, or stopped.')}
           actionLinks={<AlertActionLink onClick={() => handleReconnect()}>{t('Reconnect')}</AlertActionLink>}
         />
       )}
@@ -123,8 +136,34 @@ const AppTerminal = ({
   const [isOpen, setIsOpen] = React.useState(false);
   const terminal = React.useRef<ImperativeTerminalType>(null);
 
-  const selectedApp = appName ? consoleAppStatuses.find((app) => app.name === appName) : undefined;
-  const activeAppName = selectedApp?.status === ApplicationStatusType.ApplicationStatusRunning ? selectedApp.name : '';
+  const lifecycleOverrides = React.useMemo(
+    () => getDeviceAppLifecycleOverrides(device.metadata.annotations ?? {}),
+    [device.metadata.annotations],
+  );
+
+  const availableApps = consoleAppStatuses.filter((app) =>
+    isAppConsoleAvailable(app.status, lifecycleOverrides[app.name]),
+  );
+
+  // The app that is currently connected to the terminal.
+  let connectedApp: DeviceApplicationStatus | undefined = undefined;
+  if (appName) {
+    connectedApp = availableApps.find((app) => app.name === appName);
+  }
+  // Only select an app by default if it's the only VM app in the device, and it's available.
+  if (!connectedApp && consoleAppStatuses.length === 1 && availableApps.length === 1) {
+    connectedApp = availableApps[0];
+  }
+
+  // The app that is selected in the dropdown. It will remain selected even if the VM becomes unavailable (it's stopped, etc).
+  let selectedApp: DeviceApplicationStatus | undefined = undefined;
+  if (connectedApp) {
+    selectedApp = connectedApp;
+  } else if (appName) {
+    selectedApp = consoleAppStatuses.find((app) => app.name === appName);
+  } else if (consoleAppStatuses.length === 1) {
+    selectedApp = consoleAppStatuses[0];
+  }
 
   const onMsgReceived = React.useCallback((data: string) => {
     terminal.current?.onDataReceived(data);
@@ -133,7 +172,7 @@ const AppTerminal = ({
 
   const { sendMessage, isClosed, error, reconnect, isConnecting, disconnect } = useAppConsoleWebSocket(
     device.metadata.name || '',
-    activeAppName,
+    connectedApp?.name || '',
     currentOrganization?.id || undefined,
     onMsgReceived,
   );
@@ -168,7 +207,7 @@ const AppTerminal = ({
             setIsOpen(false);
             handleAppSelect(String(value));
           }}
-          selected={appName}
+          selected={selectedApp?.name}
           shouldFocusToggleOnSelect
           toggle={(toggleRef: React.Ref<MenuToggleElement>) => (
             <MenuToggle
@@ -183,12 +222,13 @@ const AppTerminal = ({
         >
           <SelectList>
             {consoleAppStatuses.map((app) => {
-              const isAvailable = app.status === ApplicationStatusType.ApplicationStatusRunning;
+              const desiredState = lifecycleOverrides[app.name];
+              const isAvailable = isAppConsoleAvailable(app.status, desiredState);
               return (
                 <SelectOption
                   key={app.name}
                   value={app.name}
-                  isSelected={app.name === appName}
+                  isSelected={app.name === (appName || connectedApp?.name)}
                   description={
                     isAvailable
                       ? t('Serial console · {{status}}', { status: app.status })
@@ -204,9 +244,9 @@ const AppTerminal = ({
         </Select>
       </StackItem>
       <StackItem isFilled style={{ minHeight: 0 }}>
-        {selectedApp ? (
+        {connectedApp ? (
           <AppTerminalContent
-            appStatus={selectedApp}
+            appStatus={connectedApp}
             sendMessage={sendMessage}
             isConnecting={isConnecting}
             isClosed={isClosed}
@@ -214,6 +254,15 @@ const AppTerminal = ({
             reconnect={reconnect}
             terminalRef={terminal}
           />
+        ) : selectedApp ? (
+          <Bullseye>
+            <Alert
+              variant="info"
+              isInline
+              isPlain
+              title={getAppTerminalUnavailableTitle(t, selectedApp.status, lifecycleOverrides[selectedApp.name])}
+            />
+          </Bullseye>
         ) : (
           <Bullseye>
             <Alert
diff --git a/libs/ui-components/src/components/Terminal/TerminalConnectError.tsx b/libs/ui-components/src/components/Terminal/TerminalConnectError.tsx
index 85eb3baea..65b24752f 100644
--- a/libs/ui-components/src/components/Terminal/TerminalConnectError.tsx
+++ b/libs/ui-components/src/components/Terminal/TerminalConnectError.tsx
@@ -17,6 +17,10 @@ const getAppConsoleConnectErrorMessage = (error: AppConsoleConnectError, t: TFun
       );
     case 'sessionTakenOver':
       return t('This console session was ended because another user connected to the same virtual machine.');
+    case 'appNotReady':
+      return t(
+        'The virtual machine console is unavailable at the moment. The VM may be starting, stopping, or stopped.',
+      );
     case 'forbidden':
       return t('You do not have permission to access the virtual machine console.');
     case 'notFound':
@@ -24,7 +28,7 @@ const getAppConsoleConnectErrorMessage = (error: AppConsoleConnectError, t: TFun
     case 'timeout':
       return t('Timed out connecting to the virtual machine console. The VM may still be starting.');
     case 'unknownError':
-      return t('Failed to connect to the virtual machine console.');
+      return error.detail || t('Failed to connect to the virtual machine console.');
   }
 };
 
diff --git a/libs/ui-components/src/hooks/useAppConsoleWebSocket.ts b/libs/ui-components/src/hooks/useAppConsoleWebSocket.ts
index 8a9c5de0a..523d39cbe 100644
--- a/libs/ui-components/src/hooks/useAppConsoleWebSocket.ts
+++ b/libs/ui-components/src/hooks/useAppConsoleWebSocket.ts
@@ -7,18 +7,23 @@ const APP_CONSOLE_CLOSE_REASON = 'client disconnect';
 /** WebSocket close code from the remote-access service when another client took over the session. */
 const WS_CLOSE_SESSION_TAKEN_OVER = 4001;
 
+/**
+ * WebSocket close code from the remote-access service when the VM app has no active compute workload.
+ * App is likely starting, stopping, or stopped.
+ */
+const WS_CLOSE_APP_NOT_READY = 4002;
+
 /** HTTP status embedded in the WebSocket close reason when the console session is already in use. */
 const HTTP_SESSION_IN_USE = 409;
 
+/** HTTP status when the VM app console is temporarily unavailable. */
+const HTTP_APP_NOT_READY = 503;
+
 const isErrorCloseEvent = (evt: CloseEvent) => evt.code !== 1000 && evt.code !== 1001;
 
 export type AppConsoleConnectError =
-  | { kind: 'sessionInUse' }
-  | { kind: 'sessionTakenOver' }
-  | { kind: 'forbidden' }
-  | { kind: 'notFound' }
-  | { kind: 'timeout' }
-  | { kind: 'unknownError' };
+  | { kind: 'sessionInUse' | 'sessionTakenOver' | 'appNotReady' | 'forbidden' | 'notFound' | 'timeout' }
+  | { kind: 'unknownError'; detail?: string };
 
 const closeAppConsoleWebSocket = (ws: WebSocket) => {
   if (ws.readyState === WebSocket.OPEN || ws.readyState === WebSocket.CONNECTING) {
@@ -26,18 +31,49 @@ const closeAppConsoleWebSocket = (ws: WebSocket) => {
   }
 };
 
-const parseCloseReasonStatus = (reason: string): number | undefined => {
-  const match = reason.trim().match(/^(\d{3})\b/);
+/** Parses proxy close reasons of the form "<status> <optional detail>". */
+export const parseCloseReason = (reason: string): { status?: number; detail?: string } => {
+  const trimmed = reason.trim();
+  const match = trimmed.match(/^(\d{3})(?:\s+(.*))?$/);
   if (!match) {
-    return undefined;
+    return trimmed ? { detail: trimmed } : {};
+  }
+  const status = Number.parseInt(match[1], 10);
+  const detail = match[2]?.trim();
+  if (!detail) {
+    return { status };
+  }
+  // Drop generic HTTP status text so callers can fall back to canned copy.
+  const statusText = (
+    {
+      403: 'Forbidden',
+      404: 'Not Found',
+      409: 'Conflict',
+      503: 'Service Unavailable',
+      504: 'Gateway Timeout',
+      502: 'Bad Gateway',
+    } as Record<number, string>
+  )[status];
+  if (statusText && detail.toLowerCase() === statusText.toLowerCase()) {
+    return { status };
   }
-  return Number.parseInt(match[1], 10);
+  return { status, detail };
 };
 
-const connectErrorFromHttpStatus = (status: number | undefined): AppConsoleConnectError => {
+const connectErrorFromCloseEvent = (evt: CloseEvent): AppConsoleConnectError => {
+  if (evt.code === WS_CLOSE_SESSION_TAKEN_OVER) {
+    return { kind: 'sessionTakenOver' };
+  }
+  if (evt.code === WS_CLOSE_APP_NOT_READY) {
+    return { kind: 'appNotReady' };
+  }
+  // Fall back to HTTP status code if no WebSocket close code is present.
+  const { status, detail } = parseCloseReason(evt.reason);
   switch (status) {
     case HTTP_SESSION_IN_USE:
       return { kind: 'sessionInUse' };
+    case HTTP_APP_NOT_READY:
+      return { kind: 'appNotReady' };
     case 403:
       return { kind: 'forbidden' };
     case 404:
@@ -45,15 +81,8 @@ const connectErrorFromHttpStatus = (status: number | undefined): AppConsoleConne
     case 504:
       return { kind: 'timeout' };
     default:
-      return { kind: 'unknownError' };
-  }
-};
-
-const connectErrorFromCloseEvent = (evt: CloseEvent): AppConsoleConnectError => {
-  if (evt.code === WS_CLOSE_SESSION_TAKEN_OVER) {
-    return { kind: 'sessionTakenOver' };
+      return { kind: 'unknownError', detail };
   }
-  return connectErrorFromHttpStatus(parseCloseReasonStatus(evt.reason));
 };
 
 const decodeMessageData = (data: ArrayBuffer | string): string => {
@@ -193,14 +222,15 @@ export const useAppConsoleWebSocket = (
         sessionActiveRef.current = false;
         if (isMountedRef.current) {
           setIsConnecting(false);
-          if (evt.code === WS_CLOSE_SESSION_TAKEN_OVER) {
-            setError(connectErrorFromCloseEvent(evt));
+          const connectError = connectErrorFromCloseEvent(evt);
+          if (connectError.kind === 'sessionTakenOver' || connectError.kind === 'appNotReady') {
+            setError(connectError);
             wsRef.current = undefined;
             return;
           }
           setIsClosed(true);
           if (isErrorCloseEvent(evt) && !hasReceivedMessageRef.current) {
-            setError(connectErrorFromCloseEvent(evt));
+            setError(connectError);
           }
         }
         wsRef.current = undefined;
diff --git a/libs/ui-components/src/utils/applicationLifecycle.ts b/libs/ui-components/src/utils/applicationLifecycle.ts
index 86f20bc63..00aadec4f 100644
--- a/libs/ui-components/src/utils/applicationLifecycle.ts
+++ b/libs/ui-components/src/utils/applicationLifecycle.ts
@@ -147,6 +147,14 @@ export const hasAplicationStatusMismatch = (
   return reconcileStartStatuses.includes(status);
 };
 
+/** Console is available only while status is Running and desired state is not Stopped. */
+export const isAppConsoleAvailable = (
+  status: ApplicationStatusType,
+  desiredState: ApplicationDesiredState | undefined,
+): boolean =>
+  status === ApplicationStatusType.ApplicationStatusRunning &&
+  desiredState !== ApplicationDesiredState.ApplicationDesiredStateStopped;
+
 /** Parses fleet and device lifecycle annotations; newer desiredStateVersion wins per application. */
 export const getDeviceAppLifecycleOverrides = (
   deviceAnnotations: Record<string, string> = {},
diff --git a/proxy/bridge/terminal.go b/proxy/bridge/terminal.go
index d34a39332..fdd292962 100644
--- a/proxy/bridge/terminal.go
+++ b/proxy/bridge/terminal.go
@@ -4,6 +4,7 @@ import (
 	"crypto/tls"
 	"errors"
 	"fmt"
+	"io"
 	"net/http"
 	"net/textproto"
 	"net/url"
@@ -32,6 +33,60 @@ var (
 	}
 )
 
+// maxWSCloseReasonBytes is the RFC 6455 limit for a close-frame reason (control payload
+// is at most 125 bytes, 2 of which are the status code).
+const maxWSCloseReasonBytes = 123
+
+// maxDialErrorBodyBytes caps how much of a failed Dial response body we read when building
+// the close reason for the browser.
+const maxDialErrorBodyBytes = 1024
+
+// Matches flightctl/internal/consts: machine-readable app console error signaling that the
+// VM application has no active compute workload (stopped / still starting).
+const (
+	appConsoleErrorCodeHeader   = "X-Flightctl-App-Console-Error"
+	appConsoleErrorCodeNotReady = "app-not-ready"
+	appConsoleNotReadyCloseCode = 4002
+)
+
+// truncateWSCloseReason bounds msg to fit in a WebSocket close frame reason field.
+func truncateWSCloseReason(msg string) string {
+	if len(msg) <= maxWSCloseReasonBytes {
+		return msg
+	}
+	return strings.ToValidUTF8(msg[:maxWSCloseReasonBytes], "")
+}
+
+// dialErrorCloseReason builds a close reason of the form "<status> <detail>" so the UI can
+// map the status code while still receiving the backend/agent error text.
+// Falls back to the HTTP status text when the body is empty.
+func dialErrorCloseReason(statusCode int, resp *http.Response) string {
+	detail := http.StatusText(statusCode)
+	if resp != nil && resp.Body != nil {
+		defer func() {
+			if err := resp.Body.Close(); err != nil {
+				log.Warnf("Failed to close dial error response body: %v", err)
+			}
+		}()
+		body, err := io.ReadAll(io.LimitReader(resp.Body, maxDialErrorBodyBytes))
+		if err == nil {
+			if trimmed := strings.TrimSpace(string(body)); trimmed != "" {
+				detail = trimmed
+			}
+		}
+	}
+	return truncateWSCloseReason(fmt.Sprintf("%d %s", statusCode, detail))
+}
+
+// dialErrorCloseCode picks a WebSocket close code for a failed Dial. Prefers the backend's
+// app-not-ready code (4002) over a generic internal server error.
+func dialErrorCloseCode(resp *http.Response) int {
+	if resp != nil && resp.Header.Get(appConsoleErrorCodeHeader) == appConsoleErrorCodeNotReady {
+		return appConsoleNotReadyCloseCode
+	}
+	return websocket.CloseInternalServerErr
+}
+
 type TerminalBridge struct {
 	TlsConfig *tls.Config
 }
@@ -252,10 +307,11 @@ func (t TerminalBridge) bridgeWebSocket(w http.ResponseWriter, r *http.Request,
 		}
 		log.Warnf("dial statusCode: '%v'", statusCode)
 
-		// On any backend error, upgrade the client to WebSocket to send a close frame
-		// The UI will receive a CloseEvent with a websocket code error and reason.
-		closeReason := fmt.Sprintf("%d %s", statusCode, http.StatusText(statusCode))
-		closeCode := websocket.CloseInternalServerErr
+		// On any backend error, upgrade the client to WebSocket to send a close frame.
+		// Include the response body (agent/API message) so the UI can show more than
+		// a generic status text such as "404 Not Found".
+		closeReason := dialErrorCloseReason(statusCode, resp)
+		closeCode := dialErrorCloseCode(resp)
 		upgrader := &websocket.Upgrader{
 			Subprotocols: websocket.Subprotocols(r),
 			CheckOrigin:  checkOrigin,