diff --git a/src/headless-query.ts b/src/headless-query.ts
index cc7c134c3..00816e103 100644
--- a/src/headless-query.ts
+++ b/src/headless-query.ts
@@ -38,7 +38,9 @@ async function loadExtensionModules() {
   const dispatchModule = await jiti.import(gsdExtensionPath('auto-dispatch.ts'), {}) as any
   const sessionModule = await jiti.import(gsdExtensionPath('session-status-io.ts'), {}) as any
   const prefsModule = await jiti.import(gsdExtensionPath('preferences.ts'), {}) as any
+  const autoStartModule = await jiti.import(gsdExtensionPath('auto-start.ts'), {}) as any
   return {
+    openProjectDbIfPresent: autoStartModule.openProjectDbIfPresent as (basePath: string) => Promise<void>,
     deriveState: stateModule.deriveState as (basePath: string) => Promise<GSDState>,
     resolveDispatch: dispatchModule.resolveDispatch as (opts: any) => Promise<any>,
     readAllSessionStatuses: sessionModule.readAllSessionStatuses as (basePath: string) => any[],
@@ -76,7 +78,14 @@ export interface QueryResult {
 // ─── Implementation ─────────────────────────────────────────────────────────
 
 export async function handleQuery(basePath: string): Promise<QueryResult> {
-  const { deriveState, resolveDispatch, readAllSessionStatuses, loadEffectiveGSDPreferences } = await loadExtensionModules()
+  const {
+    openProjectDbIfPresent,
+    deriveState,
+    resolveDispatch,
+    readAllSessionStatuses,
+    loadEffectiveGSDPreferences,
+  } = await loadExtensionModules()
+  await openProjectDbIfPresent(basePath)
   const state = await deriveState(basePath)
 
   // Derive next dispatch action
diff --git a/src/tests/headless-query-db-open.test.ts b/src/tests/headless-query-db-open.test.ts
new file mode 100644
index 000000000..c562455ad
--- /dev/null
+++ b/src/tests/headless-query-db-open.test.ts
@@ -0,0 +1,29 @@
+/**
+ * Regression test for #4123: headless-query must open the project DB
+ * before deriveState(), otherwise it falls back to filesystem parsing.
+ */
+
+import { test } from "node:test";
+import assert from "node:assert/strict";
+import { readFileSync } from "node:fs";
+import { join, dirname } from "node:path";
+import { fileURLToPath } from "node:url";
+
+const __dirname = dirname(fileURLToPath(import.meta.url));
+const src = readFileSync(join(__dirname, "..", "headless-query.ts"), "utf-8");
+
+test("headless-query loads openProjectDbIfPresent from extension modules (#4123)", () => {
+  assert.match(
+    src,
+    /openProjectDbIfPresent:\s*autoStartModule\.openProjectDbIfPresent/,
+    "headless-query should load openProjectDbIfPresent from auto-start.ts",
+  );
+});
+
+test("headless-query opens the DB before deriveState (#4123)", () => {
+  const openIdx = src.indexOf("await openProjectDbIfPresent(basePath)");
+  const deriveIdx = src.indexOf("const state = await deriveState(basePath)");
+  assert.ok(openIdx !== -1, "headless-query should open the project DB");
+  assert.ok(deriveIdx !== -1, "headless-query should still derive state");
+  assert.ok(openIdx < deriveIdx, "headless-query should open the DB before deriveState()");
+});