diff --git a/cli/tests/unit/tls_test.ts b/cli/tests/unit/tls_test.ts
index b2382833f7..17f2312c0e 100644
--- a/cli/tests/unit/tls_test.ts
+++ b/cli/tests/unit/tls_test.ts
@@ -1121,3 +1121,139 @@ unitTest(
     conn.close();
   },
 );
+
+// TODO(piscisaureus): use `TlsConn.handhake()` instead, once this is added to
+// the public API in Deno 1.16.
+function tlsHandshake(conn: Deno.Conn): Promise<void> {
+  // deno-lint-ignore no-explicit-any
+  const opAsync = (Deno as any).core.opAsync;
+  return opAsync("op_tls_handshake", conn.rid);
+}
+
+unitTest(
+  { permissions: { read: true, net: true } },
+  async function tlsHandshakeSuccess() {
+    const hostname = "localhost";
+    const port = getPort();
+
+    const listener = Deno.listenTls({
+      hostname,
+      port,
+      certFile: "cli/tests/testdata/tls/localhost.crt",
+      keyFile: "cli/tests/testdata/tls/localhost.key",
+    });
+    const acceptPromise = listener.accept();
+    const connectPromise = Deno.connectTls({
+      hostname,
+      port,
+      certFile: "cli/tests/testdata/tls/RootCA.crt",
+    });
+    const [conn1, conn2] = await Promise.all([acceptPromise, connectPromise]);
+    listener.close();
+
+    await Promise.all([tlsHandshake(conn1), tlsHandshake(conn2)]);
+
+    // Begin sending a 10mb blob over the TLS connection.
+    const whole = new Uint8Array(10 << 20); // 10mb.
+    whole.fill(42);
+    const sendPromise = conn1.write(whole);
+
+    // Set up the other end to receive half of the large blob.
+    const half = new Uint8Array(whole.byteLength / 2);
+    const receivePromise = readFull(conn2, half);
+
+    await tlsHandshake(conn1);
+    await tlsHandshake(conn2);
+
+    // Finish receiving the first 5mb.
+    assertEquals(await receivePromise, half.length);
+
+    // See that we can call `handshake()` in the middle of large reads and writes.
+    await tlsHandshake(conn1);
+    await tlsHandshake(conn2);
+
+    // Receive second half of large blob. Wait for the send promise and check it.
+    assertEquals(await readFull(conn2, half), half.length);
+    assertEquals(await sendPromise, whole.length);
+
+    await tlsHandshake(conn1);
+    await tlsHandshake(conn2);
+
+    await conn1.closeWrite();
+    await conn2.closeWrite();
+
+    await tlsHandshake(conn1);
+    await tlsHandshake(conn2);
+
+    conn1.close();
+    conn2.close();
+
+    async function readFull(conn: Deno.Conn, buf: Uint8Array) {
+      let offset, n;
+      for (offset = 0; offset < buf.length; offset += n) {
+        n = await conn.read(buf.subarray(offset, buf.length));
+        assert(n != null && n > 0);
+      }
+      return offset;
+    }
+  },
+);
+
+unitTest(
+  { permissions: { read: true, net: true } },
+  async function tlsHandshakeFailure() {
+    const hostname = "localhost";
+    const port = getPort();
+
+    async function server() {
+      const listener = Deno.listenTls({
+        hostname,
+        port,
+        certFile: "cli/tests/testdata/tls/localhost.crt",
+        keyFile: "cli/tests/testdata/tls/localhost.key",
+      });
+      for await (const conn of listener) {
+        for (let i = 0; i < 10; i++) {
+          // Handshake fails because the client rejects the server certificate.
+          await assertRejects(
+            () => tlsHandshake(conn),
+            Deno.errors.InvalidData,
+            "BadCertificate",
+          );
+        }
+        conn.close();
+        break;
+      }
+    }
+
+    async function connectTlsClient() {
+      const conn = await Deno.connectTls({ hostname, port });
+      // Handshake fails because the server presents a self-signed certificate.
+      await assertRejects(
+        () => tlsHandshake(conn),
+        Deno.errors.InvalidData,
+        "UnknownIssuer",
+      );
+      conn.close();
+    }
+
+    await Promise.all([server(), connectTlsClient()]);
+
+    async function startTlsClient() {
+      const tcpConn = await Deno.connect({ hostname, port });
+      const tlsConn = await Deno.startTls(tcpConn, {
+        hostname: "foo.land",
+        certFile: "cli/tests/testdata/tls/RootCA.crt",
+      });
+      // Handshake fails because hostname doesn't match the certificate.
+      await assertRejects(
+        () => tlsHandshake(tlsConn),
+        Deno.errors.InvalidData,
+        "CertNotValidForName",
+      );
+      tlsConn.close();
+    }
+
+    await Promise.all([server(), startTlsClient()]);
+  },
+);
diff --git a/ext/net/README.md b/ext/net/README.md
index cdd8923e1c..6377e79749 100644
--- a/ext/net/README.md
+++ b/ext/net/README.md
@@ -22,6 +22,7 @@ Following ops are provided:
 - "op_connect_tls"
 - "op_listen_tls"
 - "op_accept_tls"
+- "op_tls_handshake"
 - "op_http_start"
 - "op_http_request_next"
 - "op_http_request_read"
diff --git a/ext/net/io.rs b/ext/net/io.rs
index 6a93b8cf6e..6cefbde2de 100644
--- a/ext/net/io.rs
+++ b/ext/net/io.rs
@@ -1,6 +1,6 @@
 // Copyright 2018-2021 the Deno authors. All rights reserved. MIT license.
 
-use crate::ops_tls as tls;
+use crate::ops_tls::TlsStreamResource;
 use deno_core::error::not_supported;
 use deno_core::error::AnyError;
 use deno_core::op_async;
@@ -114,18 +114,6 @@ impl Resource for TcpStreamResource {
   }
 }
 
-pub type TlsStreamResource = FullDuplexResource<tls::ReadHalf, tls::WriteHalf>;
-
-impl Resource for TlsStreamResource {
-  fn name(&self) -> Cow<str> {
-    "tlsStream".into()
-  }
-
-  fn close(self: Rc<Self>) {
-    self.cancel_read_ops();
-  }
-}
-
 #[cfg(unix)]
 pub type UnixStreamResource =
   FullDuplexResource<unix::OwnedReadHalf, unix::OwnedWriteHalf>;
diff --git a/ext/net/ops_tls.rs b/ext/net/ops_tls.rs
index d6618440fb..129a702bcf 100644
--- a/ext/net/ops_tls.rs
+++ b/ext/net/ops_tls.rs
@@ -1,7 +1,6 @@
 // Copyright 2018-2021 the Deno authors. All rights reserved. MIT license.
 
 use crate::io::TcpStreamResource;
-use crate::io::TlsStreamResource;
 use crate::ops::IpAddr;
 use crate::ops::OpAddr;
 use crate::ops::OpConn;
@@ -53,6 +52,7 @@ use io::Read;
 use io::Write;
 use serde::Deserialize;
 use std::borrow::Cow;
+use std::cell::Cell;
 use std::cell::RefCell;
 use std::convert::From;
 use std::fs::File;
@@ -67,7 +67,9 @@ use std::rc::Rc;
 use std::sync::Arc;
 use std::sync::Weak;
 use tokio::io::AsyncRead;
+use tokio::io::AsyncReadExt;
 use tokio::io::AsyncWrite;
+use tokio::io::AsyncWriteExt;
 use tokio::io::ReadBuf;
 use tokio::net::TcpListener;
 use tokio::net::TcpStream;
@@ -113,6 +115,7 @@ impl From<ServerSession> for TlsSession {
 
 #[derive(Copy, Clone, Debug, Eq, PartialEq)]
 enum Flow {
+  Handshake,
   Read,
   Write,
 }
@@ -123,6 +126,7 @@ enum State {
   StreamClosed,
   TlsClosing,
   TlsClosed,
+  TlsError,
   TcpClosed,
 }
 
@@ -157,10 +161,6 @@ impl TlsStream {
     Self::new(tcp, tls)
   }
 
-  pub async fn handshake(&mut self) -> io::Result<()> {
-    poll_fn(|cx| self.inner_mut().poll_io(cx, Flow::Write)).await
-  }
-
   fn into_split(self) -> (ReadHalf, WriteHalf) {
     let shared = Shared::new(self);
     let rd = ReadHalf {
@@ -180,6 +180,14 @@ impl TlsStream {
   fn inner_mut(&mut self) -> &mut TlsStreamInner {
     self.0.as_mut().unwrap()
   }
+
+  pub async fn handshake(&mut self) -> io::Result<()> {
+    poll_fn(|cx| self.inner_mut().poll_handshake(cx)).await
+  }
+
+  fn poll_handshake(&mut self, cx: &mut Context<'_>) -> Poll<io::Result<()>> {
+    self.inner_mut().poll_handshake(cx)
+  }
 }
 
 impl AsyncRead for TlsStream {
@@ -282,20 +290,20 @@ impl TlsStreamInner {
           _ => {}
         }
 
+        // Write ciphertext to the TCP socket.
+        let mut wrapped_tcp = ImplementWriteTrait(&mut self.tcp);
+        match self.tls.write_tls(&mut wrapped_tcp) {
+          Ok(0) => {}        // Wait until the socket has enough buffer space.
+          Ok(_) => continue, // Try to send more more data immediately.
+          Err(err) if err.kind() == ErrorKind::WouldBlock => unreachable!(),
+          Err(err) => return Poll::Ready(Err(err)),
+        }
+
         // Poll whether there is space in the socket send buffer so we can flush
         // the remaining outgoing ciphertext.
         if self.tcp.poll_write_ready(cx)?.is_pending() {
           break false;
         }
-
-        // Write ciphertext to the TCP socket.
-        let mut wrapped_tcp = ImplementWriteTrait(&mut self.tcp);
-        match self.tls.write_tls(&mut wrapped_tcp) {
-          Ok(0) => unreachable!(),
-          Ok(_) => {}
-          Err(err) if err.kind() == ErrorKind::WouldBlock => {}
-          Err(err) => return Poll::Ready(Err(err)),
-        }
       };
 
       let rd_ready = loop {
@@ -304,6 +312,7 @@ impl TlsStreamInner {
             let err = Error::new(ErrorKind::UnexpectedEof, "tls handshake eof");
             return Poll::Ready(Err(err));
           }
+          State::TlsError => {}
           _ if self.tls.is_handshaking() && !self.tls.wants_read() => {
             break true;
           }
@@ -343,22 +352,36 @@ impl TlsStreamInner {
           }
         }
 
-        // Poll whether more ciphertext is available in the socket receive
-        // buffer.
-        if self.tcp.poll_read_ready(cx)?.is_pending() {
-          break false;
+        if self.rd_state != State::TlsError {
+          // Receive ciphertext from the socket.
+          let mut wrapped_tcp = ImplementReadTrait(&mut self.tcp);
+          match self.tls.read_tls(&mut wrapped_tcp) {
+            Ok(0) => {
+              // End of TCP stream.
+              self.rd_state = State::TcpClosed;
+              continue;
+            }
+            Err(err) if err.kind() == ErrorKind::WouldBlock => {
+              // Get notified when more ciphertext becomes available in the
+              // socket receive buffer.
+              if self.tcp.poll_read_ready(cx)?.is_pending() {
+                break false;
+              } else {
+                continue;
+              }
+            }
+            Err(err) => return Poll::Ready(Err(err)),
+            _ => {}
+          }
         }
 
-        // Receive ciphertext from the socket.
-        let mut wrapped_tcp = ImplementReadTrait(&mut self.tcp);
-        match self.tls.read_tls(&mut wrapped_tcp) {
-          Ok(0) => self.rd_state = State::TcpClosed,
-          Ok(_) => self
-            .tls
-            .process_new_packets()
-            .map_err(|err| Error::new(ErrorKind::InvalidData, err))?,
-          Err(err) if err.kind() == ErrorKind::WouldBlock => {}
-          Err(err) => return Poll::Ready(Err(err)),
+        // Interpret and decrypt TLS protocol data.
+        match self.tls.process_new_packets() {
+          Ok(_) => assert!(self.rd_state < State::TcpClosed),
+          Err(err) => {
+            self.rd_state = State::TlsError;
+            return Poll::Ready(Err(Error::new(ErrorKind::InvalidData, err)));
+          }
         }
       };
 
@@ -376,6 +399,7 @@ impl TlsStreamInner {
 
       let io_ready = match flow {
         _ if self.tls.is_handshaking() => false,
+        Flow::Handshake => true,
         Flow::Read => rd_ready,
         Flow::Write => wr_ready,
       };
@@ -386,6 +410,13 @@ impl TlsStreamInner {
     }
   }
 
+  fn poll_handshake(&mut self, cx: &mut Context<'_>) -> Poll<io::Result<()>> {
+    if self.tls.is_handshaking() {
+      ready!(self.poll_io(cx, Flow::Handshake))?;
+    }
+    Poll::Ready(Ok(()))
+  }
+
   fn poll_read(
     &mut self,
     cx: &mut Context<'_>,
@@ -505,6 +536,19 @@ pub struct WriteHalf {
   shared: Arc<Shared>,
 }
 
+impl WriteHalf {
+  pub async fn handshake(&mut self) -> io::Result<()> {
+    poll_fn(|cx| {
+      self
+        .shared
+        .poll_with_shared_waker(cx, Flow::Write, |mut tls, cx| {
+          tls.poll_handshake(cx)
+        })
+    })
+    .await
+  }
+}
+
 impl AsyncWrite for WriteHalf {
   fn poll_write(
     self: Pin<&mut Self>,
@@ -561,6 +605,7 @@ impl Shared {
     mut f: impl FnMut(Pin<&mut TlsStream>, &mut Context<'_>) -> R,
   ) -> R {
     match flow {
+      Flow::Handshake => unreachable!(),
       Flow::Read => self.rd_waker.register(cx.waker()),
       Flow::Write => self.wr_waker.register(cx.waker()),
     }
@@ -625,7 +670,11 @@ struct ImplementWriteTrait<'a, T>(&'a mut T);
 
 impl Write for ImplementWriteTrait<'_, TcpStream> {
   fn write(&mut self, buf: &[u8]) -> io::Result<usize> {
-    self.0.try_write(buf)
+    match self.0.try_write(buf) {
+      Ok(n) => Ok(n),
+      Err(err) if err.kind() == ErrorKind::WouldBlock => Ok(0),
+      Err(err) => Err(err),
+    }
   }
 
   fn flush(&mut self) -> io::Result<()> {
@@ -639,9 +688,78 @@ pub fn init<P: NetPermissions + 'static>() -> Vec<OpPair> {
     ("op_connect_tls", op_async(op_connect_tls::<P>)),
     ("op_listen_tls", op_sync(op_listen_tls::<P>)),
     ("op_accept_tls", op_async(op_accept_tls)),
+    ("op_tls_handshake", op_async(op_tls_handshake)),
   ]
 }
 
+#[derive(Debug)]
+pub struct TlsStreamResource {
+  rd: AsyncRefCell<ReadHalf>,
+  wr: AsyncRefCell<WriteHalf>,
+  handshake_done: Cell<bool>,
+  cancel_handle: CancelHandle, // Only read and handshake ops get canceled.
+}
+
+impl TlsStreamResource {
+  pub fn new((rd, wr): (ReadHalf, WriteHalf)) -> Self {
+    Self {
+      rd: rd.into(),
+      wr: wr.into(),
+      handshake_done: Cell::new(false),
+      cancel_handle: Default::default(),
+    }
+  }
+
+  pub fn into_inner(self) -> (ReadHalf, WriteHalf) {
+    (self.rd.into_inner(), self.wr.into_inner())
+  }
+
+  pub async fn read(
+    self: &Rc<Self>,
+    buf: &mut [u8],
+  ) -> Result<usize, AnyError> {
+    let mut rd = RcRef::map(self, |r| &r.rd).borrow_mut().await;
+    let cancel_handle = RcRef::map(self, |r| &r.cancel_handle);
+    let nread = rd.read(buf).try_or_cancel(cancel_handle).await?;
+    Ok(nread)
+  }
+
+  pub async fn write(self: &Rc<Self>, buf: &[u8]) -> Result<usize, AnyError> {
+    self.handshake().await?;
+    let mut wr = RcRef::map(self, |r| &r.wr).borrow_mut().await;
+    let nwritten = wr.write(buf).await?;
+    wr.flush().await?;
+    Ok(nwritten)
+  }
+
+  pub async fn shutdown(self: &Rc<Self>) -> Result<(), AnyError> {
+    self.handshake().await?;
+    let mut wr = RcRef::map(self, |r| &r.wr).borrow_mut().await;
+    wr.shutdown().await?;
+    Ok(())
+  }
+
+  pub async fn handshake(self: &Rc<Self>) -> Result<(), AnyError> {
+    if !self.handshake_done.get() {
+      let mut wr = RcRef::map(self, |r| &r.wr).borrow_mut().await;
+      let cancel_handle = RcRef::map(self, |r| &r.cancel_handle);
+      wr.handshake().try_or_cancel(cancel_handle).await?;
+      self.handshake_done.set(true);
+    }
+    Ok(())
+  }
+}
+
+impl Resource for TlsStreamResource {
+  fn name(&self) -> Cow<str> {
+    "tlsStream".into()
+  }
+
+  fn close(self: Rc<Self>) {
+    self.cancel_handle.cancel();
+  }
+}
+
 #[derive(Deserialize)]
 #[serde(rename_all = "camelCase")]
 pub struct ConnectTlsArgs {
@@ -1015,3 +1133,15 @@ async fn op_accept_tls(
     })),
   })
 }
+
+async fn op_tls_handshake(
+  state: Rc<RefCell<OpState>>,
+  rid: ResourceId,
+  _: (),
+) -> Result<(), AnyError> {
+  let resource = state
+    .borrow()
+    .resource_table
+    .get::<TlsStreamResource>(rid)?;
+  resource.handshake().await
+}
diff --git a/runtime/ops/http.rs b/runtime/ops/http.rs
index 58783bbbc2..683dc1a576 100644
--- a/runtime/ops/http.rs
+++ b/runtime/ops/http.rs
@@ -7,7 +7,7 @@ use deno_core::Extension;
 use deno_core::OpState;
 use deno_core::ResourceId;
 use deno_net::io::TcpStreamResource;
-use deno_net::io::TlsStreamResource;
+use deno_net::ops_tls::TlsStreamResource;
 
 pub fn init() -> Extension {
   Extension::builder()
diff --git a/runtime/ops/io.rs b/runtime/ops/io.rs
index 0687fc397f..7eb27bd125 100644
--- a/runtime/ops/io.rs
+++ b/runtime/ops/io.rs
@@ -16,8 +16,8 @@ use deno_core::Resource;
 use deno_core::ResourceId;
 use deno_core::ZeroCopyBuf;
 use deno_net::io::TcpStreamResource;
-use deno_net::io::TlsStreamResource;
 use deno_net::io::UnixStreamResource;
+use deno_net::ops_tls::TlsStreamResource;
 use std::borrow::Cow;
 use std::cell::RefCell;
 use std::io::Read;