diff --git a/apps/app/package.json b/apps/app/package.json
index 2838d2a8d..c0f4e43d4 100644
--- a/apps/app/package.json
+++ b/apps/app/package.json
@@ -18,6 +18,7 @@
     "test:events": "node scripts/events.mjs",
     "test:todos": "node scripts/todos.mjs",
     "test:permissions": "node scripts/permissions.mjs",
+    "test:openwork-selection": "bun scripts/openwork-selection.ts",
     "test:session-scope": "bun scripts/session-scope.ts",
     "test:session-switch": "node scripts/session-switch.mjs",
     "test:fs-engine": "node scripts/fs-engine.mjs",
diff --git a/apps/app/scripts/openwork-selection.ts b/apps/app/scripts/openwork-selection.ts
new file mode 100644
index 000000000..4e2c65e9e
--- /dev/null
+++ b/apps/app/scripts/openwork-selection.ts
@@ -0,0 +1,97 @@
+import assert from "node:assert/strict";
+
+const { selectOpenworkWorkspace } = await import("../src/app/workspace/openwork-selection.ts");
+
+const workspace = (id: string, directory?: string) => ({
+  id,
+  name: id,
+  path: directory ?? "",
+  preset: "remote",
+  workspaceType: "remote" as const,
+  remoteType: "openwork" as const,
+  baseUrl: `https://example.com/w/${id}/opencode`,
+  directory: directory ?? null,
+  opencode: directory ? { directory } : undefined,
+});
+
+const results = {
+  ok: true,
+  steps: [] as Array<Record<string, unknown>>,
+};
+
+async function step(name: string, fn: () => void | Promise<void>) {
+  results.steps.push({ name, status: "running" });
+  const index = results.steps.length - 1;
+
+  try {
+    await fn();
+    results.steps[index] = { name, status: "ok" };
+  } catch (error) {
+    results.ok = false;
+    results.steps[index] = {
+      name,
+      status: "error",
+      error: error instanceof Error ? error.message : String(error),
+    };
+    throw error;
+  }
+}
+
+try {
+  await step("explicit workspace id wins", () => {
+    const result = selectOpenworkWorkspace({
+      items: [workspace("ws_alpha", "/repo/a"), workspace("ws_beta", "/repo/b")],
+      workspaceId: "ws_beta",
+    });
+
+    assert.deepEqual(result, { ok: true, workspace: workspace("ws_beta", "/repo/b") });
+  });
+
+  await step("directory hint resolves normalized matches", () => {
+    const result = selectOpenworkWorkspace({
+      items: [workspace("ws_alpha", "/repo/a"), workspace("ws_beta", "/repo/b")],
+      directoryHint: "/repo/b/",
+    });
+
+    assert.deepEqual(result, { ok: true, workspace: workspace("ws_beta", "/repo/b") });
+  });
+
+  await step("single-workspace hosts still connect without extra selectors", () => {
+    const result = selectOpenworkWorkspace({
+      items: [workspace("ws_only", "/repo/a")],
+    });
+
+    assert.deepEqual(result, { ok: true, workspace: workspace("ws_only", "/repo/a") });
+  });
+
+  await step("multi-workspace hosts reject ambiguous host-only connects", () => {
+    const result = selectOpenworkWorkspace({
+      items: [workspace("ws_alpha", "/repo/a"), workspace("ws_beta", "/repo/b")],
+    });
+
+    assert.deepEqual(result, {
+      ok: false,
+      reason: "ambiguous",
+      message:
+        "OpenWork host returned multiple workspaces. Use a workspace-scoped URL (/w/ws_*) or reconnect from the specific workspace.",
+    });
+  });
+
+  await step("stale directory hints no longer silently fall back to the first workspace", () => {
+    const result = selectOpenworkWorkspace({
+      items: [workspace("ws_alpha", "/repo/a"), workspace("ws_beta", "/repo/b")],
+      directoryHint: "/repo/missing",
+    });
+
+    assert.deepEqual(result, {
+      ok: false,
+      reason: "not-found",
+      message: "OpenWork worker directory not found on that host.",
+    });
+  });
+
+  console.log(JSON.stringify(results));
+} catch {
+  console.log(JSON.stringify(results));
+  process.exitCode = 1;
+}
diff --git a/apps/app/src/app/app.tsx b/apps/app/src/app/app.tsx
index 8b352ff35..23eac7af5 100644
--- a/apps/app/src/app/app.tsx
+++ b/apps/app/src/app/app.tsx
@@ -612,7 +612,9 @@ export default function App() {
     if (!id) return false;
     const ready = await workspaceStore.activateWorkspace(id);
     if (ready) {
-      await refreshSidebarWorkspaceSessions(id).catch(() => undefined);
+      // Keep workspace activation on the critical path for correctness, but do
+      // not block session creation or prompt send on a sidebar refresh.
+      void refreshSidebarWorkspaceSessions(id).catch(() => undefined);
     }
     return ready;
   };
diff --git a/apps/app/src/app/context/workspace.ts b/apps/app/src/app/context/workspace.ts
index aeebde2d3..cb79410f1 100644
--- a/apps/app/src/app/context/workspace.ts
+++ b/apps/app/src/app/context/workspace.ts
@@ -33,6 +33,7 @@ import {
   type OpenworkServerClient,
   type OpenworkWorkspaceInfo,
 } from "../lib/openwork-server";
+import { selectOpenworkWorkspace } from "../workspace/openwork-selection";
 import { downloadDir, homeDir } from "@tauri-apps/api/path";
 import {
   engineDoctor,
@@ -816,32 +817,15 @@ export function createWorkspaceStore(options: {
     }
 
     const response = await client.listWorkspaces();
-    const items = Array.isArray(response.items) ? response.items : [];
-    const hint = normalizeDirectoryPath(input.directoryHint ?? "");
-    const selectByHint = (entry: OpenworkWorkspaceInfo) => {
-      if (!hint) return false;
-      const entryPath = normalizeDirectoryPath(
-        (entry.opencode?.directory as string | undefined) ?? (entry.path as string | undefined) ?? "",
-      );
-      return Boolean(entryPath && entryPath === hint);
-    };
-    const selectById = (entry: OpenworkWorkspaceInfo) => Boolean(requestedWorkspaceId && entry?.id === requestedWorkspaceId);
-
-    const workspaceById = requestedWorkspaceId
-      ? (items.find((item) => item?.id && selectById(item as any)) as OpenworkWorkspaceInfo | undefined)
-      : undefined;
-    if (requestedWorkspaceId && !workspaceById) {
-      throw new Error("OpenWork worker not found on that host.");
-    }
-
-    const workspaceByHint = hint
-      ? (items.find((item) => item?.id && selectByHint(item as any)) as OpenworkWorkspaceInfo | undefined)
-      : undefined;
-
-    const workspace = (workspaceById ?? workspaceByHint ?? items[0]) as OpenworkWorkspaceInfo | undefined;
-    if (!workspace?.id) {
-      throw new Error("OpenWork server did not return a worker.");
+    const selected = selectOpenworkWorkspace({
+      items: Array.isArray(response.items) ? response.items : [],
+      workspaceId: requestedWorkspaceId,
+      directoryHint: input.directoryHint ?? null,
+    });
+    if (!selected.ok) {
+      throw new Error(selected.message);
     }
+    const workspace = selected.workspace;
     const opencodeUpstreamBaseUrl = workspace.opencode?.baseUrl?.trim() ?? workspace.baseUrl?.trim() ?? "";
     if (!opencodeUpstreamBaseUrl) {
       throw new Error("OpenWork server did not provide an OpenCode URL.");
@@ -1201,7 +1185,7 @@ export function createWorkspaceStore(options: {
         const resolved = await resolveOpenworkHost({
           hostUrl,
           token,
-          workspaceId: workspace.openworkWorkspaceId ?? null,
+          workspaceId: resolveRuntimeWorkspaceLookup(workspace)?.workspaceId ?? null,
         });
         if (resolved.kind !== "openwork") {
           updateWorkspaceConnectionState(id, {
@@ -1509,7 +1493,7 @@ export function createWorkspaceStore(options: {
             const resolved = await resolveOpenworkHost({
               hostUrl,
               token,
-              workspaceId: next.openworkWorkspaceId ?? null,
+              workspaceId: resolveRuntimeWorkspaceLookup(next)?.workspaceId ?? null,
               directoryHint: next.directory ?? null,
             });
             if (resolved.kind !== "openwork") {
@@ -2792,7 +2776,7 @@ export function createWorkspaceStore(options: {
       const resolved = await resolveOpenworkHost({
         hostUrl,
         token,
-        workspaceId: workspace.openworkWorkspaceId ?? null,
+        workspaceId: resolveRuntimeWorkspaceLookup(workspace)?.workspaceId ?? null,
         directoryHint: directory || null,
       });
       if (resolved.kind !== "openwork") {
diff --git a/apps/app/src/app/workspace/openwork-selection.ts b/apps/app/src/app/workspace/openwork-selection.ts
new file mode 100644
index 000000000..cf8647260
--- /dev/null
+++ b/apps/app/src/app/workspace/openwork-selection.ts
@@ -0,0 +1,80 @@
+import type { OpenworkWorkspaceInfo } from "../lib/openwork-server";
+import { normalizeDirectoryPath } from "../utils";
+
+type OpenworkWorkspaceSelectionReason = "missing" | "not-found" | "ambiguous";
+
+export type OpenworkWorkspaceSelectionResult =
+  | {
+      ok: true;
+      workspace: OpenworkWorkspaceInfo;
+    }
+  | {
+      ok: false;
+      reason: OpenworkWorkspaceSelectionReason;
+      message: string;
+    };
+
+const workspaceDirectory = (entry: OpenworkWorkspaceInfo) =>
+  normalizeDirectoryPath((entry.opencode?.directory as string | undefined) ?? entry.directory ?? entry.path ?? "");
+
+export function selectOpenworkWorkspace(input: {
+  items: OpenworkWorkspaceInfo[];
+  workspaceId?: string | null;
+  directoryHint?: string | null;
+}): OpenworkWorkspaceSelectionResult {
+  const items = Array.isArray(input.items) ? input.items.filter((entry): entry is OpenworkWorkspaceInfo => Boolean(entry?.id)) : [];
+  const explicitWorkspaceId = input.workspaceId?.trim() ?? "";
+  const directoryHint = normalizeDirectoryPath(input.directoryHint ?? "");
+
+  if (!items.length) {
+    return {
+      ok: false,
+      reason: "missing",
+      message: "OpenWork server did not return a worker.",
+    };
+  }
+
+  if (explicitWorkspaceId) {
+    const exact = items.find((entry) => entry.id === explicitWorkspaceId);
+    if (exact) {
+      return { ok: true, workspace: exact };
+    }
+    return {
+      ok: false,
+      reason: "not-found",
+      message: "OpenWork worker not found on that host.",
+    };
+  }
+
+  if (directoryHint) {
+    const matches = items.filter((entry) => workspaceDirectory(entry) === directoryHint);
+    if (matches.length === 1) {
+      return { ok: true, workspace: matches[0] };
+    }
+    if (matches.length > 1) {
+      return {
+        ok: false,
+        reason: "ambiguous",
+        message: "OpenWork host returned multiple workspaces for that directory.",
+      };
+    }
+    if (items.length === 1) {
+      return { ok: true, workspace: items[0] };
+    }
+    return {
+      ok: false,
+      reason: "not-found",
+      message: "OpenWork worker directory not found on that host.",
+    };
+  }
+
+  if (items.length === 1) {
+    return { ok: true, workspace: items[0] };
+  }
+
+  return {
+    ok: false,
+    reason: "ambiguous",
+    message: "OpenWork host returned multiple workspaces. Use a workspace-scoped URL (/w/ws_*) or reconnect from the specific workspace.",
+  };
+}