diff --git a/codex-rs/exec-server/src/client_transport.rs b/codex-rs/exec-server/src/client_transport.rs
index 8ca1eb0280..4bdc09a80e 100644
--- a/codex-rs/exec-server/src/client_transport.rs
+++ b/codex-rs/exec-server/src/client_transport.rs
@@ -15,6 +15,7 @@ use crate::client_api::RemoteExecServerConnectArgs;
 use crate::client_api::StdioExecServerCommand;
 use crate::client_api::StdioExecServerConnectArgs;
 use crate::connection::JsonRpcConnection;
+use crate::relay::harness_connection_from_websocket;
 
 const ENVIRONMENT_CLIENT_NAME: &str = "codex-environment";
 
@@ -69,14 +70,13 @@ impl ExecServerClient {
                 source,
             })?;
 
-        Self::connect(
-            JsonRpcConnection::from_websocket(
-                stream,
-                format!("exec-server websocket {websocket_url}"),
-            ),
-            args.into(),
-        )
-        .await
+        let connection_label = format!("exec-server websocket {websocket_url}");
+        let connection = if is_rendezvous_harness_url(&websocket_url) {
+            harness_connection_from_websocket(stream, connection_label)
+        } else {
+            JsonRpcConnection::from_websocket(stream, connection_label)
+        };
+        Self::connect(connection, args.into()).await
     }
 
     pub(crate) async fn connect_stdio_command(
@@ -120,6 +120,16 @@ impl ExecServerClient {
     }
 }
 
+fn is_rendezvous_harness_url(websocket_url: &str) -> bool {
+    let Some((_path, query)) = websocket_url.split_once('?') else {
+        return false;
+    };
+    query
+        .split('&')
+        .filter_map(|pair| pair.split_once('='))
+        .any(|(key, value)| key == "role" && value == "harness")
+}
+
 fn stdio_command_process(stdio_command: &StdioExecServerCommand) -> Command {
     let mut command = Command::new(&stdio_command.program);
     command.args(&stdio_command.args);
diff --git a/codex-rs/exec-server/src/lib.rs b/codex-rs/exec-server/src/lib.rs
index d8c147127c..9fbca92d7c 100644
--- a/codex-rs/exec-server/src/lib.rs
+++ b/codex-rs/exec-server/src/lib.rs
@@ -13,6 +13,7 @@ mod local_process;
 mod process;
 mod process_id;
 mod protocol;
+mod relay;
 mod remote;
 mod remote_file_system;
 mod remote_process;
diff --git a/codex-rs/exec-server/src/relay.rs b/codex-rs/exec-server/src/relay.rs
new file mode 100644
index 0000000000..ac1dc1bc67
--- /dev/null
+++ b/codex-rs/exec-server/src/relay.rs
@@ -0,0 +1,462 @@
+use std::collections::HashMap;
+
+use base64::Engine;
+use base64::engine::general_purpose::STANDARD as BASE64_STANDARD;
+use codex_app_server_protocol::JSONRPCMessage;
+use futures::SinkExt;
+use futures::StreamExt;
+use serde::Deserialize;
+use serde::Serialize;
+use tokio::io::AsyncRead;
+use tokio::io::AsyncWrite;
+use tokio::sync::mpsc;
+use tokio::sync::watch;
+use tokio_tungstenite::WebSocketStream;
+use tokio_tungstenite::tungstenite::Message;
+use tracing::debug;
+use tracing::warn;
+use uuid::Uuid;
+
+use crate::ExecServerError;
+use crate::connection::CHANNEL_CAPACITY;
+use crate::connection::JsonRpcConnection;
+use crate::connection::JsonRpcConnectionEvent;
+use crate::connection::JsonRpcTransport;
+use crate::server::ConnectionProcessor;
+
+const RELAY_MESSAGE_FRAME_VERSION: u32 = 1;
+#[derive(Debug, Clone, Copy, Eq, PartialEq, Deserialize, Serialize)]
+#[serde(rename_all = "snake_case")]
+enum RelayMessageFrameKind {
+    Data,
+    Ack,
+    Resume,
+    Reset,
+    Heartbeat,
+}
+
+#[derive(Debug, Clone, Deserialize, Serialize)]
+#[serde(rename_all = "camelCase")]
+struct RelayMessageFrame {
+    version: u32,
+    stream_id: String,
+    kind: RelayMessageFrameKind,
+    ack: u32,
+    ack_bits: u32,
+    #[serde(skip_serializing_if = "Option::is_none")]
+    seq: Option<u32>,
+    #[serde(skip_serializing_if = "Option::is_none")]
+    segment_index: Option<u32>,
+    #[serde(skip_serializing_if = "Option::is_none")]
+    segment_count: Option<u32>,
+    #[serde(skip_serializing_if = "Option::is_none")]
+    payload_base64: Option<String>,
+    #[serde(skip_serializing_if = "Option::is_none")]
+    reason: Option<String>,
+}
+
+impl RelayMessageFrame {
+    fn data(stream_id: String, seq: u32, payload: Vec<u8>) -> Self {
+        Self {
+            version: RELAY_MESSAGE_FRAME_VERSION,
+            stream_id,
+            kind: RelayMessageFrameKind::Data,
+            ack: 0,
+            ack_bits: 0,
+            seq: Some(seq),
+            segment_index: Some(0),
+            segment_count: Some(1),
+            payload_base64: Some(BASE64_STANDARD.encode(payload)),
+            reason: None,
+        }
+    }
+
+    fn resume(stream_id: String) -> Self {
+        Self {
+            version: RELAY_MESSAGE_FRAME_VERSION,
+            stream_id,
+            kind: RelayMessageFrameKind::Resume,
+            ack: 0,
+            ack_bits: 0,
+            seq: None,
+            segment_index: None,
+            segment_count: None,
+            payload_base64: None,
+            reason: None,
+        }
+    }
+
+    fn validate(&self) -> Result<(), ExecServerError> {
+        if self.version != RELAY_MESSAGE_FRAME_VERSION {
+            return Err(ExecServerError::Protocol(format!(
+                "unsupported relay message frame version {}",
+                self.version
+            )));
+        }
+        if self.stream_id.trim().is_empty() {
+            return Err(ExecServerError::Protocol(
+                "relay message frame is missing streamId".to_string(),
+            ));
+        }
+        if self.kind == RelayMessageFrameKind::Data
+            && (self.seq.is_none()
+                || self.segment_index != Some(0)
+                || self.segment_count != Some(1)
+                || self.payload_base64.is_none())
+        {
+            return Err(ExecServerError::Protocol(
+                "relay data message frame is missing required fields".to_string(),
+            ));
+        }
+        if self.kind == RelayMessageFrameKind::Reset && self.reason.is_none() {
+            return Err(ExecServerError::Protocol(
+                "relay reset message frame is missing reason".to_string(),
+            ));
+        }
+        Ok(())
+    }
+
+    fn into_jsonrpc_message(self) -> Result<JSONRPCMessage, ExecServerError> {
+        self.validate()?;
+        if self.kind != RelayMessageFrameKind::Data {
+            return Err(ExecServerError::Protocol(
+                "expected relay data message frame".to_string(),
+            ));
+        }
+        let payload = BASE64_STANDARD
+            .decode(self.payload_base64.unwrap_or_default())
+            .map_err(|err| ExecServerError::Protocol(format!("invalid payloadBase64: {err}")))?;
+        serde_json::from_slice(&payload).map_err(ExecServerError::Json)
+    }
+}
+
+fn serialize_relay_message_frame(frame: &RelayMessageFrame) -> Result<String, ExecServerError> {
+    serde_json::to_string(frame).map_err(ExecServerError::Json)
+}
+
+fn jsonrpc_payload(message: &JSONRPCMessage) -> Result<Vec<u8>, ExecServerError> {
+    serde_json::to_vec(message).map_err(ExecServerError::Json)
+}
+
+pub(crate) fn harness_connection_from_websocket<S>(
+    stream: WebSocketStream<S>,
+    connection_label: String,
+) -> JsonRpcConnection
+where
+    S: AsyncRead + AsyncWrite + Unpin + Send + 'static,
+{
+    let stream_id = Uuid::new_v4().to_string();
+    let (mut websocket_writer, mut websocket_reader) = stream.split();
+    let (outgoing_tx, mut outgoing_rx) = mpsc::channel(CHANNEL_CAPACITY);
+    let (incoming_tx, incoming_rx) = mpsc::channel(CHANNEL_CAPACITY);
+    let (disconnected_tx, disconnected_rx) = watch::channel(false);
+
+    let reader_label = connection_label;
+    let reader_stream_id = stream_id.clone();
+    let incoming_tx_for_reader = incoming_tx;
+    let disconnected_tx_for_reader = disconnected_tx.clone();
+    let reader_task = tokio::spawn(async move {
+        loop {
+            match websocket_reader.next().await {
+                Some(Ok(Message::Text(text))) => {
+                    let frame = match serde_json::from_str::<RelayMessageFrame>(text.as_ref()) {
+                        Ok(frame) => frame,
+                        Err(err) => {
+                            let _ = incoming_tx_for_reader
+                                .send(JsonRpcConnectionEvent::MalformedMessage {
+                                    reason: format!(
+                                        "failed to parse relay message frame from {reader_label}: {err}"
+                                    ),
+                                })
+                                .await;
+                            continue;
+                        }
+                    };
+                    if frame.stream_id != reader_stream_id {
+                        continue;
+                    }
+                    match frame.kind {
+                        RelayMessageFrameKind::Data => match frame.into_jsonrpc_message() {
+                            Ok(message) => {
+                                if incoming_tx_for_reader
+                                    .send(JsonRpcConnectionEvent::Message(message))
+                                    .await
+                                    .is_err()
+                                {
+                                    break;
+                                }
+                            }
+                            Err(err) => {
+                                let _ = incoming_tx_for_reader
+                                    .send(JsonRpcConnectionEvent::MalformedMessage {
+                                        reason: err.to_string(),
+                                    })
+                                    .await;
+                            }
+                        },
+                        RelayMessageFrameKind::Reset => {
+                            let _ = disconnected_tx_for_reader.send(true);
+                            let _ = incoming_tx_for_reader
+                                .send(JsonRpcConnectionEvent::Disconnected {
+                                    reason: frame.reason,
+                                })
+                                .await;
+                            break;
+                        }
+                        RelayMessageFrameKind::Ack
+                        | RelayMessageFrameKind::Resume
+                        | RelayMessageFrameKind::Heartbeat => {}
+                    }
+                }
+                Some(Ok(Message::Close(_))) | None => {
+                    let _ = disconnected_tx_for_reader.send(true);
+                    let _ = incoming_tx_for_reader
+                        .send(JsonRpcConnectionEvent::Disconnected { reason: None })
+                        .await;
+                    break;
+                }
+                Some(Ok(Message::Ping(_) | Message::Pong(_) | Message::Frame(_))) => {}
+                Some(Ok(Message::Binary(_))) => {
+                    let _ = incoming_tx_for_reader
+                        .send(JsonRpcConnectionEvent::MalformedMessage {
+                            reason: "relay exec-server transport expects JSON text frames"
+                                .to_string(),
+                        })
+                        .await;
+                }
+                Some(Err(err)) => {
+                    let _ = disconnected_tx_for_reader.send(true);
+                    let _ = incoming_tx_for_reader
+                        .send(JsonRpcConnectionEvent::Disconnected {
+                            reason: Some(format!(
+                                "failed to read relay websocket frame from {reader_label}: {err}"
+                            )),
+                        })
+                        .await;
+                    break;
+                }
+            }
+        }
+    });
+
+    let writer_task = tokio::spawn(async move {
+        let resume = RelayMessageFrame::resume(stream_id.clone());
+        match serialize_relay_message_frame(&resume) {
+            Ok(encoded) => {
+                if websocket_writer
+                    .send(Message::Text(encoded.into()))
+                    .await
+                    .is_err()
+                {
+                    let _ = disconnected_tx.send(true);
+                    return;
+                }
+            }
+            Err(err) => {
+                warn!("failed to serialize relay resume frame: {err}");
+                let _ = disconnected_tx.send(true);
+                return;
+            }
+        }
+
+        let mut next_seq = 0u32;
+        while let Some(message) = outgoing_rx.recv().await {
+            let payload = match jsonrpc_payload(&message) {
+                Ok(payload) => payload,
+                Err(err) => {
+                    warn!("failed to serialize JSON-RPC payload for relay transport: {err}");
+                    break;
+                }
+            };
+            let frame = RelayMessageFrame::data(stream_id.clone(), next_seq, payload);
+            next_seq = next_seq.wrapping_add(1);
+            match serialize_relay_message_frame(&frame) {
+                Ok(encoded) => {
+                    if websocket_writer
+                        .send(Message::Text(encoded.into()))
+                        .await
+                        .is_err()
+                    {
+                        let _ = disconnected_tx.send(true);
+                        break;
+                    }
+                }
+                Err(err) => {
+                    warn!("failed to serialize relay data message frame: {err}");
+                    let _ = disconnected_tx.send(true);
+                    break;
+                }
+            }
+        }
+    });
+
+    JsonRpcConnection {
+        outgoing_tx,
+        incoming_rx,
+        disconnected_rx,
+        task_handles: vec![reader_task, writer_task],
+        transport: JsonRpcTransport::Plain,
+    }
+}
+
+pub(crate) async fn run_multiplexed_executor<S>(
+    stream: WebSocketStream<S>,
+    processor: ConnectionProcessor,
+) where
+    S: AsyncRead + AsyncWrite + Unpin + Send + 'static,
+{
+    let (mut websocket_writer, mut websocket_reader) = stream.split();
+    let (physical_outgoing_tx, mut physical_outgoing_rx) =
+        mpsc::channel::<String>(CHANNEL_CAPACITY);
+    let writer_task = tokio::spawn(async move {
+        while let Some(encoded) = physical_outgoing_rx.recv().await {
+            if websocket_writer
+                .send(Message::Text(encoded.into()))
+                .await
+                .is_err()
+            {
+                break;
+            }
+        }
+    });
+
+    let mut streams: HashMap<String, VirtualStream> = HashMap::new();
+    loop {
+        let frame = match websocket_reader.next().await {
+            Some(Ok(Message::Text(text))) => {
+                match serde_json::from_str::<RelayMessageFrame>(text.as_ref()) {
+                    Ok(frame) => frame,
+                    Err(err) => {
+                        warn!("dropping malformed relay message frame from harness: {err}");
+                        continue;
+                    }
+                }
+            }
+            Some(Ok(Message::Close(_))) | None => break,
+            Some(Ok(Message::Ping(_) | Message::Pong(_) | Message::Frame(_))) => continue,
+            Some(Ok(Message::Binary(_))) => {
+                warn!("dropping non-text relay message frame from harness");
+                continue;
+            }
+            Some(Err(err)) => {
+                debug!("multiplexed executor websocket read failed: {err}");
+                break;
+            }
+        };
+
+        if let Err(err) = frame.validate() {
+            warn!("dropping invalid relay message frame: {err}");
+            continue;
+        }
+
+        match frame.kind {
+            RelayMessageFrameKind::Data => {
+                let stream_id = frame.stream_id.clone();
+                let message = match frame.into_jsonrpc_message() {
+                    Ok(message) => message,
+                    Err(err) => {
+                        warn!("dropping malformed relay data message frame: {err}");
+                        continue;
+                    }
+                };
+                let stream = streams.entry(stream_id.clone()).or_insert_with(|| {
+                    spawn_virtual_stream(
+                        stream_id.clone(),
+                        processor.clone(),
+                        physical_outgoing_tx.clone(),
+                    )
+                });
+                if stream
+                    .incoming_tx
+                    .send(JsonRpcConnectionEvent::Message(message))
+                    .await
+                    .is_err()
+                {
+                    streams.remove(&stream_id);
+                }
+            }
+            RelayMessageFrameKind::Reset => {
+                if let Some(stream) = streams.remove(&frame.stream_id) {
+                    stream.disconnect(frame.reason).await;
+                }
+            }
+            RelayMessageFrameKind::Ack
+            | RelayMessageFrameKind::Resume
+            | RelayMessageFrameKind::Heartbeat => {}
+        }
+    }
+
+    for (_stream_id, stream) in streams {
+        stream.disconnect(/*reason*/ None).await;
+    }
+    drop(physical_outgoing_tx);
+    let _ = writer_task.await;
+}
+
+struct VirtualStream {
+    incoming_tx: mpsc::Sender<JsonRpcConnectionEvent>,
+    disconnected_tx: watch::Sender<bool>,
+}
+
+impl VirtualStream {
+    async fn disconnect(self, reason: Option<String>) {
+        let _ = self.disconnected_tx.send(true);
+        let _ = self
+            .incoming_tx
+            .send(JsonRpcConnectionEvent::Disconnected { reason })
+            .await;
+    }
+}
+
+fn spawn_virtual_stream(
+    stream_id: String,
+    processor: ConnectionProcessor,
+    physical_outgoing_tx: mpsc::Sender<String>,
+) -> VirtualStream {
+    let (json_outgoing_tx, mut json_outgoing_rx) = mpsc::channel(CHANNEL_CAPACITY);
+    let (incoming_tx, incoming_rx) = mpsc::channel(CHANNEL_CAPACITY);
+    let (disconnected_tx, disconnected_rx) = watch::channel(false);
+
+    let writer_stream_id = stream_id;
+    let writer_task = tokio::spawn(async move {
+        let mut next_seq = 0u32;
+        while let Some(message) = json_outgoing_rx.recv().await {
+            let payload = match jsonrpc_payload(&message) {
+                Ok(payload) => payload,
+                Err(err) => {
+                    warn!("failed to serialize virtual stream JSON-RPC payload: {err}");
+                    break;
+                }
+            };
+            let frame = RelayMessageFrame::data(writer_stream_id.clone(), next_seq, payload);
+            next_seq = next_seq.wrapping_add(1);
+            match serialize_relay_message_frame(&frame) {
+                Ok(encoded) => {
+                    if physical_outgoing_tx.send(encoded).await.is_err() {
+                        break;
+                    }
+                }
+                Err(err) => {
+                    warn!("failed to serialize virtual stream relay message frame: {err}");
+                    break;
+                }
+            }
+        }
+    });
+
+    let connection = JsonRpcConnection {
+        outgoing_tx: json_outgoing_tx,
+        incoming_rx,
+        disconnected_rx,
+        task_handles: vec![writer_task],
+        transport: JsonRpcTransport::Plain,
+    };
+    tokio::spawn(async move {
+        processor.run_connection(connection).await;
+    });
+
+    VirtualStream {
+        incoming_tx,
+        disconnected_tx,
+    }
+}
diff --git a/codex-rs/exec-server/src/remote.rs b/codex-rs/exec-server/src/remote.rs
index bb22105c19..4fbdef77b0 100644
--- a/codex-rs/exec-server/src/remote.rs
+++ b/codex-rs/exec-server/src/remote.rs
@@ -11,7 +11,7 @@ use codex_utils_rustls_provider::ensure_rustls_crypto_provider;
 
 use crate::ExecServerError;
 use crate::ExecServerRuntimePaths;
-use crate::connection::JsonRpcConnection;
+use crate::relay::run_multiplexed_executor;
 use crate::server::ConnectionProcessor;
 
 pub const CODEX_EXEC_SERVER_REMOTE_BEARER_TOKEN_ENV_VAR: &str =
@@ -150,12 +150,7 @@ pub async fn run_remote_executor(
         match connect_async(response.url.as_str()).await {
             Ok((websocket, _)) => {
                 backoff = Duration::from_secs(1);
-                processor
-                    .run_connection(JsonRpcConnection::from_websocket(
-                        websocket,
-                        "remote exec-server websocket".to_string(),
-                    ))
-                    .await;
+                run_multiplexed_executor(websocket, processor.clone()).await;
             }
             Err(err) => {
                 warn!("failed to connect remote exec-server websocket: {err}");