diff --git a/lib/_http_agent.js b/lib/_http_agent.js
index 2d52ea3143b3cd..c4430e86ec3aca 100644
--- a/lib/_http_agent.js
+++ b/lib/_http_agent.js
@@ -34,6 +34,7 @@ const EventEmitter = require('events');
 let debug = require('internal/util/debuglog').debuglog('http', (fn) => {
   debug = fn;
 });
+const { AsyncResource } = require('async_hooks');
 const { async_id_symbol } = require('internal/async_hooks').symbols;
 const {
   codes: {
@@ -47,6 +48,7 @@ const { validateNumber } = require('internal/validators');
 
 const kOnKeylog = Symbol('onkeylog');
 const kRequestOptions = Symbol('requestOptions');
+const kRequestAsyncResource = Symbol('requestAsyncResource');
 // New Agent code.
 
 // The largest departure from the previous implementation is that
@@ -127,7 +129,17 @@ function Agent(options) {
     const requests = this.requests[name];
     if (requests && requests.length) {
       const req = requests.shift();
-      setRequestSocket(this, req, socket);
+      const reqAsyncRes = req[kRequestAsyncResource];
+      if (reqAsyncRes) {
+        // Run request within the original async context.
+        reqAsyncRes.runInAsyncScope(() => {
+          asyncResetHandle(socket);
+          setRequestSocket(this, req, socket);
+        });
+        req[kRequestAsyncResource] = null;
+      } else {
+        setRequestSocket(this, req, socket);
+      }
       if (requests.length === 0) {
         delete this.requests[name];
       }
@@ -253,14 +265,7 @@ Agent.prototype.addRequest = function addRequest(req, options, port/* legacy */,
   const sockLen = freeLen + this.sockets[name].length;
 
   if (socket) {
-    // Guard against an uninitialized or user supplied Socket.
-    const handle = socket._handle;
-    if (handle && typeof handle.asyncReset === 'function') {
-      // Assign the handle a new asyncId and run any destroy()/init() hooks.
-      handle.asyncReset(new ReusedHandle(handle.getProviderType(), handle));
-      socket[async_id_symbol] = handle.getAsyncId();
-    }
-
+    asyncResetHandle(socket);
     this.reuseSocket(socket, req);
     setRequestSocket(this, req, socket);
     this.sockets[name].push(socket);
@@ -284,6 +289,8 @@ Agent.prototype.addRequest = function addRequest(req, options, port/* legacy */,
 
     // Used to create sockets for pending requests from different origin
     req[kRequestOptions] = options;
+    // Used to capture the original async context.
+    req[kRequestAsyncResource] = new AsyncResource('QueuedRequest');
 
     this.requests[name].push(req);
   }
@@ -493,6 +500,16 @@ function setRequestSocket(agent, req, socket) {
   socket.setTimeout(req.timeout);
 }
 
+function asyncResetHandle(socket) {
+  // Guard against an uninitialized or user supplied Socket.
+  const handle = socket._handle;
+  if (handle && typeof handle.asyncReset === 'function') {
+    // Assign the handle a new asyncId and run any destroy()/init() hooks.
+    handle.asyncReset(new ReusedHandle(handle.getProviderType(), handle));
+    socket[async_id_symbol] = handle.getAsyncId();
+  }
+}
+
 module.exports = {
   Agent,
   globalAgent: new Agent()
diff --git a/test/async-hooks/test-async-local-storage-http-agent.js b/test/async-hooks/test-async-local-storage-http-agent.js
new file mode 100644
index 00000000000000..1de535aa709687
--- /dev/null
+++ b/test/async-hooks/test-async-local-storage-http-agent.js
@@ -0,0 +1,35 @@
+'use strict';
+const common = require('../common');
+const assert = require('assert');
+const { AsyncLocalStorage } = require('async_hooks');
+const http = require('http');
+
+const asyncLocalStorage = new AsyncLocalStorage();
+
+const agent = new http.Agent({
+  maxSockets: 1
+});
+
+const N = 3;
+let responses = 0;
+
+const server = http.createServer(common.mustCall((req, res) => {
+  res.end('ok');
+}, N));
+
+server.listen(0, common.mustCall(() => {
+  const port = server.address().port;
+
+  for (let i = 0; i < N; i++) {
+    asyncLocalStorage.run(i, () => {
+      http.get({ agent, port }, common.mustCall((res) => {
+        assert.strictEqual(asyncLocalStorage.getStore(), i);
+        if (++responses === N) {
+          server.close();
+          agent.destroy();
+        }
+        res.resume();
+      }));
+    });
+  }
+}));
diff --git a/test/async-hooks/test-http-agent-handle-reuse-parallel.js b/test/async-hooks/test-http-agent-handle-reuse-parallel.js
new file mode 100644
index 00000000000000..cd73b3ed2cb61c
--- /dev/null
+++ b/test/async-hooks/test-http-agent-handle-reuse-parallel.js
@@ -0,0 +1,92 @@
+'use strict';
+// Flags: --expose-internals
+const common = require('../common');
+const initHooks = require('./init-hooks');
+const { checkInvocations } = require('./hook-checks');
+const assert = require('assert');
+const { async_id_symbol } = require('internal/async_hooks').symbols;
+const http = require('http');
+
+// Checks that the async resource used in init in case of a reused handle
+// is not reused. Test is based on parallel\test-async-hooks-http-agent.js.
+
+const hooks = initHooks();
+hooks.enable();
+
+const reqAsyncIds = [];
+let socket;
+let responses = 0;
+
+// Make sure a single socket is transparently reused for 2 requests.
+const agent = new http.Agent({
+  keepAlive: true,
+  keepAliveMsecs: Infinity,
+  maxSockets: 1
+});
+
+const verifyRequest = (idx) => (res) => {
+  reqAsyncIds[idx] = res.socket[async_id_symbol];
+  assert.ok(reqAsyncIds[idx] > 0, `${reqAsyncIds[idx]} > 0`);
+  if (socket) {
+    // Check that both requests share their socket.
+    assert.strictEqual(res.socket, socket);
+  } else {
+    socket = res.socket;
+  }
+
+  res.on('data', common.mustCallAtLeast(() => {}));
+  res.on('end', common.mustCall(() => {
+    if (++responses === 2) {
+      // Clean up to let the event loop stop.
+      server.close();
+      agent.destroy();
+    }
+  }));
+};
+
+const server = http.createServer(common.mustCall((req, res) => {
+  req.once('data', common.mustCallAtLeast(() => {
+    res.writeHead(200, { 'Content-Type': 'text/plain' });
+    res.write('foo');
+  }));
+  req.on('end', common.mustCall(() => {
+    res.end('bar');
+  }));
+}, 2)).listen(0, common.mustCall(() => {
+  const port = server.address().port;
+  const payload = 'hello world';
+
+  // First request.
+  const r1 = http.request({
+    agent, port, method: 'POST'
+  }, common.mustCall(verifyRequest(0)));
+  r1.end(payload);
+
+  // Second request. Sent in parallel with the first one.
+  const r2 = http.request({
+    agent, port, method: 'POST'
+  }, common.mustCall(verifyRequest(1)));
+  r2.end(payload);
+}));
+
+
+process.on('exit', onExit);
+
+function onExit() {
+  hooks.disable();
+  hooks.sanityCheck();
+  const activities = hooks.activities;
+
+  // Verify both invocations
+  const first = activities.filter((x) => x.uid === reqAsyncIds[0])[0];
+  checkInvocations(first, { init: 1, destroy: 1 }, 'when process exits');
+
+  const second = activities.filter((x) => x.uid === reqAsyncIds[1])[0];
+  checkInvocations(second, { init: 1, destroy: 1 }, 'when process exits');
+
+  // Verify reuse handle has been wrapped
+  assert.strictEqual(first.type, second.type);
+  assert.ok(first.handle !== second.handle, 'Resource reused');
+  assert.ok(first.handle === second.handle.handle,
+            'Resource not wrapped correctly');
+}
diff --git a/test/async-hooks/test-http-agent-handle-reuse.js b/test/async-hooks/test-http-agent-handle-reuse-serial.js
similarity index 98%
rename from test/async-hooks/test-http-agent-handle-reuse.js
rename to test/async-hooks/test-http-agent-handle-reuse-serial.js
index 4db83bec54a7bf..bbc7183d6e72ca 100644
--- a/test/async-hooks/test-http-agent-handle-reuse.js
+++ b/test/async-hooks/test-http-agent-handle-reuse-serial.js
@@ -7,7 +7,7 @@ const assert = require('assert');
 const { async_id_symbol } = require('internal/async_hooks').symbols;
 const http = require('http');
 
-// Checks that the async resource used in init in case of a resused handle
+// Checks that the async resource used in init in case of a reused handle
 // is not reused. Test is based on parallel\test-async-hooks-http-agent.js.
 
 const hooks = initHooks();