diff --git a/src/main/runtime/orca-runtime-create-agent-session.ts b/src/main/runtime/orca-runtime-create-agent-session.ts
index 4c42117fb9e..103e76ec146 100644
--- a/src/main/runtime/orca-runtime-create-agent-session.ts
+++ b/src/main/runtime/orca-runtime-create-agent-session.ts
@@ -36,7 +36,7 @@ export abstract class OrcaRuntimeWithCreateAgentSession extends OrcaRuntimeWithG
     agentTeamsEnv?: Record<string, string>
   ): Record<string, string>
 
-  abstract getAuthoritativeWindow(): BrowserWindow
+  abstract getAuthoritativeWindow(missingWindowMessage?: string): BrowserWindow
 
   abstract waitForTerminalHandle(tabId: string, timeoutMs?: number): Promise<string>
 
diff --git a/src/main/runtime/orca-runtime-create-terminal-desktop.test.ts b/src/main/runtime/orca-runtime-create-terminal-desktop.test.ts
new file mode 100644
index 00000000000..d78120de8c9
--- /dev/null
+++ b/src/main/runtime/orca-runtime-create-terminal-desktop.test.ts
@@ -0,0 +1,10 @@
+import { expect, it } from 'vitest'
+import { wireHeadlessServeRuntime } from './orca-runtime-test-scenario-builders.spec'
+
+it('tells a workspace-less create on a windowless host to pass --worktree', async () => {
+  const runtime = wireHeadlessServeRuntime()
+
+  await expect(runtime.createTerminal(undefined, { title: 'probe' })).rejects.toThrow(
+    /No workspace was given or found.*Pass --worktree.*No terminal was created\./
+  )
+})
diff --git a/src/main/runtime/orca-runtime-create-terminal-desktop.ts b/src/main/runtime/orca-runtime-create-terminal-desktop.ts
index 774b5f8acd1..6a656ebf79d 100644
--- a/src/main/runtime/orca-runtime-create-terminal-desktop.ts
+++ b/src/main/runtime/orca-runtime-create-terminal-desktop.ts
@@ -3,6 +3,10 @@ import * as dependencies from './orca-runtime-create-terminal-dependencies'
 import type { OrcaRuntimeWithCreateTerminal } from './terminal/launch/terminal-create'
 import type { RuntimeTerminalPresentation } from '../../shared/runtime-types'
 
+// Without a window, the missing piece the caller can supply is the workspace, so name that.
+const NO_WORKSPACE_OR_WINDOW_MESSAGE =
+  'No workspace was given or found for this terminal, and this Orca host has no open app window to create one in. Pass --worktree to choose a workspace. No terminal was created.'
+
 // A create with no workspace lands in whatever the window is showing, so only the window can make it.
 export async function createDesktopTerminal(
   runtime: OrcaRuntimeWithCreateTerminal,
@@ -17,7 +21,7 @@ export async function createDesktopTerminal(
   }
   opts = applyRemoteViewerLaunchEnv(opts, opts.terminalImageViewerSupported)
   runtime.assertGraphReady()
-  const win = runtime.getAuthoritativeWindow()
+  const win = runtime.getAuthoritativeWindow(NO_WORKSPACE_OR_WINDOW_MESSAGE)
   const requestId = dependencies.randomUUID()
   const reply = await new Promise<{ tabId: string; title: string }>((resolve, reject) => {
     const timer = setTimeout(() => {
diff --git a/src/main/runtime/orca-runtime-resolve-waiter.ts b/src/main/runtime/orca-runtime-resolve-waiter.ts
index c90d5b081e4..ef2693bb8c4 100644
--- a/src/main/runtime/orca-runtime-resolve-waiter.ts
+++ b/src/main/runtime/orca-runtime-resolve-waiter.ts
@@ -25,10 +25,10 @@ export abstract class OrcaRuntimeWithResolveWaiter extends OrcaRuntimeWithResolv
     return `${tabId}::${leafId}`
   }
 
-  getAuthoritativeWindow(): BrowserWindow {
+  getAuthoritativeWindow(missingWindowMessage = 'No renderer window available'): BrowserWindow {
     const win = this.getAvailableAuthoritativeWindow()
     if (!win || win.isDestroyed()) {
-      throw new Error('No renderer window available')
+      throw new Error(missingWindowMessage)
     }
     return win
   }
diff --git a/src/main/runtime/terminal/driver/terminal-driver-resources.ts b/src/main/runtime/terminal/driver/terminal-driver-resources.ts
index 3aa1eb0cf72..25edbeee6ed 100644
--- a/src/main/runtime/terminal/driver/terminal-driver-resources.ts
+++ b/src/main/runtime/terminal/driver/terminal-driver-resources.ts
@@ -51,7 +51,7 @@ export abstract class OrcaRuntimeWithTerminalDrivers extends OrcaRuntimeWithFitO
     repoId?: string
     hostId?: ExecutionHostId
   }): BrowserNetworkExecutionHost | Promise<BrowserNetworkExecutionHost>
-  abstract getAuthoritativeWindow(): BrowserWindow
+  abstract getAuthoritativeWindow(missingWindowMessage?: string): BrowserWindow
   protected abstract getAvailableAuthoritativeWindow(): BrowserWindow | null
   protected abstract markHeadlessBrowserSessionTabActive(
     worktreeId: string | undefined,