diff --git a/packages/tui/src/app.tsx b/packages/tui/src/app.tsx
index 57f372ef709a..c0dcbc36ee71 100644
--- a/packages/tui/src/app.tsx
+++ b/packages/tui/src/app.tsx
@@ -476,6 +476,7 @@ function App(props: { onSnapshot?: () => Promise<string[]>; pluginHost: TuiPlugi
   })
 
   const args = useArgs()
+  const startupPrompt = args.prompt ? { input: args.prompt, parts: [] } : undefined
   onMount(() => {
     batch(() => {
       if (args.agent) local.agent.set(args.agent)
@@ -493,6 +494,7 @@ function App(props: { onSnapshot?: () => Promise<string[]>; pluginHost: TuiPlugi
         route.navigate({
           type: "session",
           sessionID: args.sessionID,
+          prompt: startupPrompt,
         })
       }
     })
@@ -510,13 +512,13 @@ function App(props: { onSnapshot?: () => Promise<string[]>; pluginHost: TuiPlugi
       if (args.fork) {
         void sdk.client.session.fork({ sessionID: match }).then((result) => {
           if (result.data?.id) {
-            route.navigate({ type: "session", sessionID: result.data.id })
+            route.navigate({ type: "session", sessionID: result.data.id, prompt: startupPrompt })
           } else {
             toast.show({ message: "Failed to fork session", variant: "error" })
           }
         })
       } else {
-        route.navigate({ type: "session", sessionID: match })
+        route.navigate({ type: "session", sessionID: match, prompt: startupPrompt })
       }
     }
   })
@@ -530,7 +532,7 @@ function App(props: { onSnapshot?: () => Promise<string[]>; pluginHost: TuiPlugi
     forked = true
     void sdk.client.session.fork({ sessionID: args.sessionID }).then((result) => {
       if (result.data?.id) {
-        route.navigate({ type: "session", sessionID: result.data.id })
+        route.navigate({ type: "session", sessionID: result.data.id, prompt: startupPrompt })
       } else {
         toast.show({ message: "Failed to fork session", variant: "error" })
       }
diff --git a/packages/tui/src/component/prompt/startup.ts b/packages/tui/src/component/prompt/startup.ts
new file mode 100644
index 000000000000..37fee6d48bb8
--- /dev/null
+++ b/packages/tui/src/component/prompt/startup.ts
@@ -0,0 +1,23 @@
+import type { PromptInfo } from "./history"
+import type { PromptRef } from "."
+
+export function createStartupPrompt(value: PromptInfo | undefined) {
+  let ref: PromptRef | undefined
+  let seeded = false
+  let submitted = false
+
+  return {
+    bind(next: PromptRef | undefined) {
+      ref = next
+      if (!value || !next || seeded) return
+      seeded = true
+      next.set(value)
+    },
+    submitWhenReady(ready: boolean) {
+      if (!value || !ref || !ready || submitted) return
+      if (ref.current.input !== value.input) return
+      submitted = true
+      ref.submit()
+    },
+  }
+}
diff --git a/packages/tui/src/routes/home.tsx b/packages/tui/src/routes/home.tsx
index d4145e2d87be..a734ed50e53f 100644
--- a/packages/tui/src/routes/home.tsx
+++ b/packages/tui/src/routes/home.tsx
@@ -12,6 +12,7 @@ import { useEditorContext } from "../context/editor"
 import { useTerminalDimensions } from "@opentui/solid"
 import { useTuiConfig } from "../config"
 import { HomeSessionDestinationProvider } from "./home/session-destination"
+import { createStartupPrompt } from "../component/prompt/startup"
 
 let once = false
 const placeholder = {
@@ -35,7 +36,7 @@ export function Home() {
     if (configured === "auto") return Math.max(75, Math.floor(dimensions().width * 0.7))
     return configured ?? 75
   })
-  let sent = false
+  const startupPrompt = createStartupPrompt(args.prompt ? { input: args.prompt, parts: [] } : undefined)
 
   onMount(() => {
     editor.clearSelection()
@@ -51,20 +52,14 @@ export function Home() {
       return
     }
     if (!args.prompt) return
-    r.set({ input: args.prompt, parts: [] })
+    startupPrompt.bind(r)
     once = true
   }
 
   // Wait for sync and model store to be ready before auto-submitting --prompt
   createEffect(() => {
     const r = ref()
-    if (sent) return
-    if (!r) return
-    if (!sync.ready || !local.model.ready) return
-    if (!args.prompt) return
-    if (r.current.input !== args.prompt) return
-    sent = true
-    r.submit()
+    startupPrompt.submitWhenReady(!!r && sync.ready && local.model.ready)
   })
 
   return (
diff --git a/packages/tui/src/routes/session/index.tsx b/packages/tui/src/routes/session/index.tsx
index 6d77b0ea58fd..34d9bc80350d 100644
--- a/packages/tui/src/routes/session/index.tsx
+++ b/packages/tui/src/routes/session/index.tsx
@@ -27,6 +27,7 @@ import { Spinner } from "../../component/spinner"
 import { createSyntaxStyleMemo, generateSubtleSyntax, selectedForeground, useTheme } from "../../context/theme"
 import { BoxRenderable, ScrollBoxRenderable, addDefaultParsers, TextAttributes, RGBA } from "@opentui/core"
 import { Prompt, type PromptRef } from "../../component/prompt"
+import { createStartupPrompt } from "../../component/prompt/startup"
 import type {
   AssistantMessage,
   Part,
@@ -275,6 +276,7 @@ export function Session() {
   const toast = useToast()
   const sdk = useSDK()
   const editor = useEditorContext()
+  const [sessionReady, setSessionReady] = createSignal(false)
 
   createEffect(() => {
     const sessionID = route.sessionID
@@ -304,6 +306,7 @@ export function Session() {
       }
       editor.reconnect(result.data.directory)
       await sync.session.sync(sessionID)
+      if (route.sessionID === sessionID) setSessionReady(true)
       if (route.sessionID === sessionID && scroll) scroll.scrollBy(100_000)
     })().catch((error) => {
       if (route.sessionID !== sessionID) return
@@ -333,16 +336,21 @@ export function Session() {
     }
   })
 
-  let seeded = false
   let scroll: ScrollBoxRenderable
   let prompt: PromptRef | undefined
+  const [startupRef, setStartupRef] = createSignal<PromptRef>()
+  const startupPrompt = createStartupPrompt(route.prompt)
   const bind = (r: PromptRef | undefined) => {
     prompt = r
     promptRef.set(r)
-    if (seeded || !route.prompt || !r) return
-    seeded = true
-    r.set(route.prompt)
+    setStartupRef(() => r)
+    startupPrompt.bind(r)
   }
+
+  createEffect(() => {
+    startupRef()
+    startupPrompt.submitWhenReady(sessionReady() && sync.ready && local.model.ready)
+  })
   const keymap = useOpencodeKeymap()
   const dialog = useDialog()
   const renderer = useRenderer()
diff --git a/packages/tui/test/cli/tui/startup-prompt.test.ts b/packages/tui/test/cli/tui/startup-prompt.test.ts
new file mode 100644
index 000000000000..165e2332a802
--- /dev/null
+++ b/packages/tui/test/cli/tui/startup-prompt.test.ts
@@ -0,0 +1,72 @@
+import { expect, test } from "bun:test"
+import type { PromptRef } from "../../../src/component/prompt"
+import type { PromptInfo } from "../../../src/component/prompt/history"
+import { createStartupPrompt } from "../../../src/component/prompt/startup"
+
+function promptRef(input: {
+  current(): PromptInfo
+  set(value: PromptInfo): void
+  submit(): void
+}): PromptRef {
+  return {
+    get current() {
+      return input.current()
+    },
+    get focused() {
+      return false
+    },
+    set: input.set,
+    submit: input.submit,
+    reset() {},
+    blur() {},
+    focus() {},
+  }
+}
+
+test("seeds and submits a startup prompt exactly once after readiness", () => {
+  const calls = {
+    set: 0,
+    submit: 0,
+  }
+  let current: PromptInfo = { input: "", parts: [] }
+  const ref = promptRef({
+    current: () => current,
+    set(value) {
+      calls.set++
+      current = value
+    },
+    submit() {
+      calls.submit++
+    },
+  })
+  const startup = createStartupPrompt({ input: "continue the work", parts: [] })
+
+  startup.bind(ref)
+  startup.bind(ref)
+  startup.submitWhenReady(false)
+  startup.submitWhenReady(true)
+  startup.submitWhenReady(true)
+
+  expect(calls).toEqual({ set: 1, submit: 1 })
+})
+
+test("does not submit after the seeded prompt has been edited", () => {
+  let current: PromptInfo = { input: "", parts: [] }
+  let submits = 0
+  const ref = promptRef({
+    current: () => current,
+    set(value) {
+      current = value
+    },
+    submit() {
+      submits++
+    },
+  })
+  const startup = createStartupPrompt({ input: "continue the work", parts: [] })
+
+  startup.bind(ref)
+  current = { input: "user edit", parts: [] }
+  startup.submitWhenReady(true)
+
+  expect(submits).toBe(0)
+})