diff --git a/src/app/api/tools/agent-bridge/upstream-ca/route.ts b/src/app/api/tools/agent-bridge/upstream-ca/route.ts
index ab7cedc9a5..8056f4fa7b 100644
--- a/src/app/api/tools/agent-bridge/upstream-ca/route.ts
+++ b/src/app/api/tools/agent-bridge/upstream-ca/route.ts
@@ -4,10 +4,12 @@
  * LOCAL_ONLY: registered in routeGuard.ts
  *
  * Persistence: <dataDir>/mitm/upstream-ca.path  (one-line text file)
- * At runtime, calling configureUpstreamCa() with the stored path activates it.
+ * After persisting, configureUpstreamCa() is called immediately so the new CA
+ * takes effect without a reboot. Spec: plan 11 §4.7.
  */
 import { AgentBridgeUpstreamCaPostSchema } from "@/shared/schemas/agentBridge";
 import { resolveMitmDataDir } from "@/mitm/dataDir";
+import { configureUpstreamCa } from "@/mitm/upstreamTrust";
 import path from "path";
 import fs from "fs";
 import { sanitizeErrorMessage } from "@omniroute/open-sse/utils/error";
@@ -72,9 +74,18 @@ export async function POST(request: Request): Promise<Response> {
 
   try {
     writeStoredCaPath(caPath);
-    return Response.json({ ok: true, path: caPath });
   } catch (err) {
     const msg = sanitizeErrorMessage(err instanceof Error ? err.message : String(err));
     return createErrorResponse({ status: 500, message: msg });
   }
+
+  // Activate the new CA immediately so it takes effect without a reboot.
+  try {
+    configureUpstreamCa(caPath);
+  } catch (err) {
+    const msg = sanitizeErrorMessage(err instanceof Error ? err.message : String(err));
+    return createErrorResponse({ status: 400, message: msg });
+  }
+
+  return Response.json({ ok: true, path: caPath });
 }
diff --git a/src/mitm/manager.ts b/src/mitm/manager.ts
index ce7c84c2f4..8058f5fe2e 100644
--- a/src/mitm/manager.ts
+++ b/src/mitm/manager.ts
@@ -11,6 +11,7 @@ import type { AgentId, DetectionResult, MitmTarget } from "./types.ts";
 import { getAllAgentBridgeStates } from "@/lib/db/agentBridgeState.ts";
 import { listCustomHosts } from "@/lib/db/inspectorCustomHosts.ts";
 import { getUserBypassPatterns } from "@/lib/db/agentBridgeBypass.ts";
+import { configureUpstreamCa } from "./upstreamTrust.ts";
 import { createLogger } from "@/shared/utils/logger.ts";
 
 const log = createLogger("mitm-manager");
@@ -35,6 +36,18 @@ export function clearCachedPassword(): void {
 const PID_FILE = path.join(resolveMitmDataDir(), "mitm", ".mitm.pid");
 const TARGETS_JSON_FILE = path.join(resolveMitmDataDir(), "mitm", "targets.json");
 const BYPASS_JSON_FILE = path.join(resolveMitmDataDir(), "mitm", "bypass.json");
+const CA_PATH_FILE = path.join(resolveMitmDataDir(), "mitm", "upstream-ca.path");
+
+/** Read the persisted upstream CA path written by the POST upstream-ca route handler. */
+function readStoredUpstreamCaPath(): string | null {
+  try {
+    if (!fs.existsSync(CA_PATH_FILE)) return null;
+    const raw = fs.readFileSync(CA_PATH_FILE, "utf8").trim();
+    return raw || null;
+  } catch {
+    return null;
+  }
+}
 
 /**
  * Write the canonical `targets.json` consumed by `server.cjs` at startup.
@@ -211,6 +224,22 @@ export async function startMitm(
     log.error({ err }, "Failed to write bypass.json (continuing)");
   }
 
+  // 0c. Apply upstream CA certificate (env var wins over stored path).
+  //     Spec: plan 11 §4.7 + acceptance criterion §12 #18.
+  try {
+    const storedCaPath = readStoredUpstreamCaPath();
+    const activeCaPath = process.env.AGENTBRIDGE_UPSTREAM_CA_CERT || storedCaPath;
+    if (activeCaPath) {
+      configureUpstreamCa(activeCaPath);
+      log.info({ caPath: activeCaPath }, "Upstream CA certificate configured");
+    }
+  } catch (err) {
+    log.error(
+      { err },
+      `AGENTBRIDGE_UPSTREAM_CA_CERT path invalid: ${(err as Error).message ?? err} (continuing without custom CA)`
+    );
+  }
+
   // 1. Generate SSL certificate if not exists
   const certPath = path.join(resolveMitmDataDir(), "mitm", "server.crt");
   if (!fs.existsSync(certPath)) {
diff --git a/tests/unit/mitm-upstream-ca-wiring.test.ts b/tests/unit/mitm-upstream-ca-wiring.test.ts
new file mode 100644
index 0000000000..a98c3688a6
--- /dev/null
+++ b/tests/unit/mitm-upstream-ca-wiring.test.ts
@@ -0,0 +1,212 @@
+/**
+ * Tests for R5-1: AGENTBRIDGE_UPSTREAM_CA_CERT wiring.
+ *
+ * Verifies that:
+ *  1. startMitm() reads the env var path with higher priority than the stored path.
+ *  2. startMitm() falls back to the stored path when no env var is set.
+ *  3. startMitm() continues boot when configureUpstreamCa throws (invalid path).
+ *  4. The POST /api/tools/agent-bridge/upstream-ca handler persists the path and
+ *     calls configureUpstreamCa(), returning 400 when the file does not exist.
+ *  5. Error responses from the POST route do not leak stack traces (Hard Rule #12).
+ *
+ * Plan reference: 11-agent-bridge.plan.md §4.7, acceptance criterion §12 #18.
+ *
+ * Note on undici: configureUpstreamCa() loads undici lazily via createRequire.
+ * The undici CacheStorage constructor fails in Node.js <22 test environments
+ * (webidl.util.markAsUncloneable is not a function).  To avoid that, tests
+ * that must call configureUpstreamCa use a non-existent path so the function
+ * throws before reaching the undici import, or they verify the path-selection
+ * logic without calling through to undici.
+ */
+import test from "node:test";
+import assert from "node:assert/strict";
+import fs from "node:fs";
+import os from "node:os";
+import path from "node:path";
+
+// ── test isolation: dedicated DATA_DIR ────────────────────────────────────────
+const TEST_DATA_DIR = fs.mkdtempSync(
+  path.join(os.tmpdir(), "omniroute-mitm-upstream-ca-wiring-")
+);
+process.env.DATA_DIR = TEST_DATA_DIR;
+
+// Ensure the mitm subdir exists for CA path file writes.
+fs.mkdirSync(path.join(TEST_DATA_DIR, "mitm"), { recursive: true });
+
+// A real PEM-like file that exists on disk (content doesn't matter for path-exists checks).
+const REAL_PEM = path.join(TEST_DATA_DIR, "test-ca.pem");
+fs.writeFileSync(REAL_PEM, "-----BEGIN CERTIFICATE-----\nfake\n-----END CERTIFICATE-----\n");
+
+const CA_PATH_FILE = path.join(TEST_DATA_DIR, "mitm", "upstream-ca.path");
+
+// ── helpers ───────────────────────────────────────────────────────────────────
+function writeStoredCaPath(caPath: string): void {
+  fs.writeFileSync(CA_PATH_FILE, caPath + "\n");
+}
+
+function readStoredCaPath(): string | null {
+  try {
+    if (!fs.existsSync(CA_PATH_FILE)) return null;
+    const raw = fs.readFileSync(CA_PATH_FILE, "utf8").trim();
+    return raw || null;
+  } catch {
+    return null;
+  }
+}
+
+function clearStoredCaPath(): void {
+  try { fs.unlinkSync(CA_PATH_FILE); } catch { /* ignore */ }
+}
+
+// ── path-selection logic tests ────────────────────────────────────────────────
+// These mirror exactly the startMitm() 0c block logic without spawning processes
+// or loading undici.
+
+test("startMitm CA wiring — env var takes precedence over stored path", () => {
+  clearStoredCaPath();
+  writeStoredCaPath("/stored/path.pem");
+
+  const envVar = "/env/path.pem";
+  const storedCaPath = readStoredCaPath();
+  const activeCaPath = envVar || storedCaPath;
+
+  assert.equal(activeCaPath, "/env/path.pem", "env var path should win");
+});
+
+test("startMitm CA wiring — falls back to stored path when no env var", () => {
+  clearStoredCaPath();
+  writeStoredCaPath(REAL_PEM);
+
+  const envVar = "";
+  const storedCaPath = readStoredCaPath();
+  const activeCaPath = envVar || storedCaPath;
+
+  assert.equal(activeCaPath, REAL_PEM, "should fall back to stored path");
+});
+
+test("startMitm CA wiring — activeCaPath is null when neither env var nor stored path", () => {
+  clearStoredCaPath();
+
+  const envVar = "";
+  const storedCaPath = readStoredCaPath();
+  const activeCaPath = envVar || storedCaPath;
+
+  assert.equal(activeCaPath, null, "activeCaPath should be null when nothing is set");
+});
+
+test("startMitm CA wiring — configureUpstreamCa called with bad path does not crash (try/catch)", async () => {
+  // Simulates the try/catch wrapper in startMitm() 0c block.
+  // configureUpstreamCa throws for a non-existent path; we verify the error
+  // message is safe (no stack trace) and that boot would continue.
+  const { configureUpstreamCa } = await import("../../src/mitm/upstreamTrust.ts");
+
+  const badPath = "/nonexistent/path/that/wont/exist/ca.pem";
+  let threw = false;
+  let caughtMsg = "";
+  try {
+    configureUpstreamCa(badPath);
+  } catch (err) {
+    threw = true;
+    caughtMsg = (err as Error).message;
+  }
+
+  // The function throws — startMitm wraps this in try/catch, so boot continues.
+  assert.ok(threw, "configureUpstreamCa should throw for non-existent path");
+  assert.ok(!caughtMsg.includes("\n    at "), "error message must not include stack trace lines");
+  assert.ok(caughtMsg.includes("AGENTBRIDGE_UPSTREAM_CA_CERT"), "error message should include env var label");
+});
+
+test("startMitm CA wiring — configureUpstreamCa no-op for undefined path", async () => {
+  const { configureUpstreamCa: configureUpstreamCaNoop } = await import("../../src/mitm/upstreamTrust.ts");
+  // undefined / empty should never load undici — safe to call in tests.
+  assert.doesNotThrow(() => configureUpstreamCaNoop(undefined));
+  assert.doesNotThrow(() => configureUpstreamCaNoop(""));
+});
+
+// ── POST route wiring tests ───────────────────────────────────────────────────
+
+test("POST upstream-ca route — returns 400 when file does not exist", async () => {
+  const { POST } = await import(
+    "../../src/app/api/tools/agent-bridge/upstream-ca/route.ts"
+  );
+
+  const badPath = "/definitely/does/not/exist/ca.pem";
+  const req = new Request("http://localhost/api/tools/agent-bridge/upstream-ca", {
+    method: "POST",
+    headers: { "content-type": "application/json" },
+    body: JSON.stringify({ path: badPath }),
+  });
+
+  const res = await POST(req);
+  assert.equal(res.status, 400, "should return 400 for non-existent file");
+
+  const data = await res.json();
+  const messageStr = JSON.stringify(data);
+  assert.ok(!messageStr.includes("\n    at "), "error response must not contain stack trace");
+  assert.ok(!messageStr.includes(".ts:"), "error response must not expose .ts file paths");
+});
+
+test("POST upstream-ca route — persists path to upstream-ca.path file on valid request", async () => {
+  // We need a file that passes fs.existsSync but note: configureUpstreamCa will
+  // try to load undici with our fake cert.  In Node.js <22 undici CacheStorage
+  // throws.  The route catches configureUpstreamCa errors and returns 400.
+  // So the persistence happens before the configureUpstreamCa call — writeStoredCaPath
+  // is called first in its own try/catch, then configureUpstreamCa is called.
+  // If configureUpstreamCa fails (undici incompatibility), the route returns 400
+  // even though the path was already persisted.
+  //
+  // This test verifies that the file was persisted before configureUpstreamCa
+  // was attempted, by checking the CA_PATH_FILE exists after the response.
+
+  clearStoredCaPath();
+  const { POST } = await import(
+    "../../src/app/api/tools/agent-bridge/upstream-ca/route.ts"
+  );
+
+  const req = new Request("http://localhost/api/tools/agent-bridge/upstream-ca", {
+    method: "POST",
+    headers: { "content-type": "application/json" },
+    body: JSON.stringify({ path: REAL_PEM }),
+  });
+
+  const res = await POST(req);
+
+  // Either 200 (undici loaded ok) or 400 (undici fails in this test env).
+  assert.ok(
+    res.status === 200 || res.status === 400,
+    `expected 200 or 400 but got ${res.status}`
+  );
+  // The file should have been written (persistence step happened).
+  assert.ok(fs.existsSync(CA_PATH_FILE), "upstream-ca.path should be written before configureUpstreamCa");
+  assert.equal(fs.readFileSync(CA_PATH_FILE, "utf8").trim(), REAL_PEM);
+});
+
+test("POST upstream-ca route — error response does not leak stack trace when configureUpstreamCa throws", async () => {
+  const { POST } = await import(
+    "../../src/app/api/tools/agent-bridge/upstream-ca/route.ts"
+  );
+
+  const badPath = "/nonexistent/for/configureUpstreamCa/ca.pem";
+  const req = new Request("http://localhost/api/tools/agent-bridge/upstream-ca", {
+    method: "POST",
+    headers: { "content-type": "application/json" },
+    body: JSON.stringify({ path: badPath }),
+  });
+
+  const res = await POST(req);
+  assert.equal(res.status, 400);
+
+  const data = await res.json();
+  const str = JSON.stringify(data);
+  assert.ok(!str.includes("\n    at "), "sanitized error must not include stack trace");
+});
+
+// ── cleanup ───────────────────────────────────────────────────────────────────
+
+test.after(() => {
+  try {
+    fs.rmSync(TEST_DATA_DIR, { recursive: true, force: true });
+  } catch {
+    // ignore
+  }
+});