diff --git a/Package.resolved b/Package.resolved
index db15534..f9b79b3 100644
--- a/Package.resolved
+++ b/Package.resolved
@@ -1,5 +1,5 @@
 {
-  "originHash" : "22b3726bc4e4c6e9c04ac97cb08a82967feb39960a93d2909768a16e11576748",
+  "originHash" : "fe99b8634d39cad3971bde2180657a2bf711968e2e9cf5e3823bc51ea1530663",
   "pins" : [
     {
       "identity" : "antlr4",
@@ -10,6 +10,24 @@
         "version" : "4.13.2"
       }
     },
+    {
+      "identity" : "cirruslabs_tart-guest-agent_apple_swift",
+      "kind" : "remoteSourceControl",
+      "location" : "https://buf.build/gen/swift/git/1.28.2-00000000000000-dfeb75ad2b39.1/cirruslabs_tart-guest-agent_apple_swift.git",
+      "state" : {
+        "revision" : "3e13bec2dd36788e80a2e5a2022d44d4a1f373cf",
+        "version" : "1.28.2-00000000000000-dfeb75ad2b39.1"
+      }
+    },
+    {
+      "identity" : "cirruslabs_tart-guest-agent_grpc_swift",
+      "kind" : "remoteSourceControl",
+      "location" : "https://buf.build/gen/swift/git/1.24.2-00000000000000-dfeb75ad2b39.1/cirruslabs_tart-guest-agent_grpc_swift.git",
+      "state" : {
+        "branch" : "1.24.2-00000000000000-dfeb75ad2b39.1",
+        "revision" : "5b6ff43b580fe435f0a174e137e2b197759a7170"
+      }
+    },
     {
       "identity" : "dynamic",
       "kind" : "remoteSourceControl",
@@ -19,6 +37,15 @@
         "revision" : "772883073d044bc754d401cabb6574624eb3778f"
       }
     },
+    {
+      "identity" : "grpc-swift",
+      "kind" : "remoteSourceControl",
+      "location" : "https://github.com/grpc/grpc-swift.git",
+      "state" : {
+        "revision" : "8c5e99d0255c373e0330730d191a3423c57373fb",
+        "version" : "1.24.2"
+      }
+    },
     {
       "identity" : "semaphore",
       "kind" : "remoteSourceControl",
@@ -64,6 +91,33 @@
         "version" : "1.2.0"
       }
     },
+    {
+      "identity" : "swift-collections",
+      "kind" : "remoteSourceControl",
+      "location" : "https://github.com/apple/swift-collections.git",
+      "state" : {
+        "revision" : "671108c96644956dddcd89dd59c203dcdb36cec7",
+        "version" : "1.1.4"
+      }
+    },
+    {
+      "identity" : "swift-http-structured-headers",
+      "kind" : "remoteSourceControl",
+      "location" : "https://github.com/apple/swift-http-structured-headers.git",
+      "state" : {
+        "revision" : "db6eea3692638a65e2124990155cd220c2915903",
+        "version" : "1.3.0"
+      }
+    },
+    {
+      "identity" : "swift-http-types",
+      "kind" : "remoteSourceControl",
+      "location" : "https://github.com/apple/swift-http-types.git",
+      "state" : {
+        "revision" : "a0a57e949a8903563aba4615869310c0ebf14c03",
+        "version" : "1.4.0"
+      }
+    },
     {
       "identity" : "swift-log",
       "kind" : "remoteSourceControl",
@@ -73,6 +127,51 @@
         "version" : "1.6.1"
       }
     },
+    {
+      "identity" : "swift-nio",
+      "kind" : "remoteSourceControl",
+      "location" : "https://github.com/apple/swift-nio.git",
+      "state" : {
+        "revision" : "34d486b01cd891297ac615e40d5999536a1e138d",
+        "version" : "2.83.0"
+      }
+    },
+    {
+      "identity" : "swift-nio-extras",
+      "kind" : "remoteSourceControl",
+      "location" : "https://github.com/apple/swift-nio-extras.git",
+      "state" : {
+        "revision" : "f1f6f772198bee35d99dd145f1513d8581a54f2c",
+        "version" : "1.26.0"
+      }
+    },
+    {
+      "identity" : "swift-nio-http2",
+      "kind" : "remoteSourceControl",
+      "location" : "https://github.com/apple/swift-nio-http2.git",
+      "state" : {
+        "revision" : "4281466512f63d1bd530e33f4aa6993ee7864be0",
+        "version" : "1.36.0"
+      }
+    },
+    {
+      "identity" : "swift-nio-ssl",
+      "kind" : "remoteSourceControl",
+      "location" : "https://github.com/apple/swift-nio-ssl.git",
+      "state" : {
+        "revision" : "4b38f35946d00d8f6176fe58f96d83aba64b36c7",
+        "version" : "2.31.0"
+      }
+    },
+    {
+      "identity" : "swift-nio-transport-services",
+      "kind" : "remoteSourceControl",
+      "location" : "https://github.com/apple/swift-nio-transport-services.git",
+      "state" : {
+        "revision" : "cd1e89816d345d2523b11c55654570acd5cd4c56",
+        "version" : "1.24.0"
+      }
+    },
     {
       "identity" : "swift-numerics",
       "kind" : "remoteSourceControl",
@@ -82,6 +181,15 @@
         "version" : "1.0.2"
       }
     },
+    {
+      "identity" : "swift-protobuf",
+      "kind" : "remoteSourceControl",
+      "location" : "https://github.com/apple/swift-protobuf.git",
+      "state" : {
+        "revision" : "ebc7251dd5b37f627c93698e4374084d98409633",
+        "version" : "1.28.2"
+      }
+    },
     {
       "identity" : "swift-retry",
       "kind" : "remoteSourceControl",
@@ -100,6 +208,15 @@
         "version" : "1.8.0"
       }
     },
+    {
+      "identity" : "swift-system",
+      "kind" : "remoteSourceControl",
+      "location" : "https://github.com/apple/swift-system.git",
+      "state" : {
+        "revision" : "a34201439c74b53f0fd71ef11741af7e7caf01e1",
+        "version" : "1.4.2"
+      }
+    },
     {
       "identity" : "swift-xattr",
       "kind" : "remoteSourceControl",
diff --git a/Package.swift b/Package.swift
index ed82911..bed3be8 100644
--- a/Package.swift
+++ b/Package.swift
@@ -24,6 +24,8 @@ let package = Package(
     .package(url: "https://github.com/groue/Semaphore", from: "0.0.8"),
     .package(url: "https://github.com/fumoboy007/swift-retry", from: "0.2.3"),
     .package(url: "https://github.com/jozefizso/swift-xattr", from: "3.0.0"),
+    .package(url: "https://github.com/grpc/grpc-swift.git", .upToNextMajor(from: "1.24.2")),
+    .package(url: "https://buf.build/gen/swift/git/1.24.2-00000000000000-dfeb75ad2b39.1/cirruslabs_tart-guest-agent_grpc_swift.git", revision: "1.24.2-00000000000000-dfeb75ad2b39.1"),
   ],
   targets: [
     .executableTarget(name: "tart", dependencies: [
@@ -40,6 +42,8 @@ let package = Package(
       .product(name: "Semaphore", package: "Semaphore"),
       .product(name: "DMRetry", package: "swift-retry"),
       .product(name: "XAttr", package: "swift-xattr"),
+      .product(name: "GRPC", package: "grpc-swift"),
+      .product(name: "Cirruslabs_TartGuestAgent_Grpc_Swift", package: "cirruslabs_tart-guest-agent_grpc_swift"),
     ], exclude: [
       "OCI/Reference/Makefile",
       "OCI/Reference/Reference.g4",
diff --git a/Sources/tart/Commands/Exec.swift b/Sources/tart/Commands/Exec.swift
new file mode 100644
index 0000000..65ef02b
--- /dev/null
+++ b/Sources/tart/Commands/Exec.swift
@@ -0,0 +1,168 @@
+import ArgumentParser
+import Foundation
+import NIOPosix
+import GRPC
+import Cirruslabs_TartGuestAgent_Grpc_Swift
+
+struct ExecCustomExitCodeError: Error {
+  let exitCode: Int32
+}
+
+struct Exec: AsyncParsableCommand {
+  static var configuration = CommandConfiguration(abstract: "Execute a command in a running VM")
+
+  @Argument(help: "VM name", completion: .custom(completeLocalMachines))
+  var name: String
+
+  @Flag(name: [.customShort("i")], help: "Attach host's standard input to a remote command")
+  var interactive: Bool = false
+
+  @Flag(name: [.customShort("t")], help: "Allocate a remote pseudo-terminal (PTY)")
+  var tty: Bool = false
+
+  @Argument(parsing: .captureForPassthrough, help: "Command to execute")
+  var command: [String]
+
+  func run() async throws {
+    // We only have withThrowingDiscardingTaskGroup available starting from macOS 14
+    if #unavailable(macOS 14) {
+      throw RuntimeError.Generic("\"tart exec\" is only available on macOS 14 (Sonoma) or newer")
+    }
+
+    // Open VM's directory
+    let vmDir = try VMStorageLocal().open(name)
+
+    // Ensure that the VM is running
+    if try !vmDir.running() {
+      throw RuntimeError.VMNotRunning(name)
+    }
+
+    // Create a gRPC channel connected to the VM's control socket
+    let group = MultiThreadedEventLoopGroup(numberOfThreads: 1)
+    defer {
+      try! group.syncShutdownGracefully()
+    }
+
+    let channel = try GRPCChannelPool.with(
+      target: .unixDomainSocket(vmDir.controlSocketURL.path()),
+      transportSecurity: .plaintext,
+      eventLoopGroup: group,
+    )
+    defer {
+      try! channel.close().wait()
+    }
+
+    // Switch controlling terminal into raw mode when remote pseudo-terminal is requested
+    var state: State? = nil
+
+    if tty && Term.IsTerminal() {
+      state = try Term.MakeRaw()
+    }
+    defer {
+      // Restore terminal to its initial state
+      if let state {
+        try! Term.Restore(state)
+      }
+    }
+
+    // Execute a command in a running VM
+    let agentAsyncClient = AgentAsyncClient(channel: channel)
+    let execCall = agentAsyncClient.makeExecCall()
+
+    try await execCall.requestStream.send(.with {
+      $0.type = .command(.with {
+        $0.name = command[0]
+        $0.args = Array(command.dropFirst(1))
+        $0.interactive = interactive
+        $0.tty = tty
+        $0.terminalSize = .with {
+          let (width, height) = try! Term.GetSize()
+
+          $0.cols = UInt32(width)
+          $0.rows = UInt32(height)
+        }
+      })
+    })
+
+    // Process command events and optionally send our standard input and/or terminal dimensions
+    try await withThrowingTaskGroup { group in
+      // Stream host's standard input if interactive mode is enabled
+      if interactive {
+        let stdinStream = AsyncStream<Data> { continuation in
+          let handle = FileHandle.standardInput
+
+          handle.readabilityHandler = { handle in
+            let data = handle.availableData
+
+            continuation.yield(data)
+
+            if data.isEmpty {
+              continuation.finish()
+            }
+          }
+        }
+
+        group.addTask {
+          for await stdinData in stdinStream {
+            try await execCall.requestStream.send(.with {
+              $0.type = .standardInput(.with {
+                $0.data = stdinData
+              })
+            })
+          }
+        }
+      }
+
+      // Stream host's terminal dimensions if pseudo-terminal is requested
+      signal(SIGWINCH, SIG_IGN)
+      let sigwinchSrc = DispatchSource.makeSignalSource(signal: SIGWINCH)
+      sigwinchSrc.activate()
+
+      if tty {
+        let terminalDimensionsStream = AsyncStream { continuation in
+          sigwinchSrc.setEventHandler {
+            continuation.yield(try! Term.GetSize())
+          }
+        }
+
+        group.addTask {
+          for await (width, height) in terminalDimensionsStream {
+            try await execCall.requestStream.send(.with {
+              $0.type = .terminalResize(.with {
+                $0.cols = UInt32(width)
+                $0.rows = UInt32(height)
+              })
+            })
+          }
+        }
+      }
+
+      // Process command events
+      group.addTask {
+        for try await response in execCall.responseStream {
+          switch response.type {
+          case .standardOutput(let ioChunk):
+            try FileHandle.standardOutput.write(contentsOf: ioChunk.data)
+          case .standardError(let ioChunk):
+            try FileHandle.standardError.write(contentsOf: ioChunk.data)
+          case .exit(let exit):
+            throw ExecCustomExitCodeError(exitCode: exit.code)
+          default:
+            // Unknown event, do nothing
+            continue
+          }
+        }
+      }
+
+      while !group.isEmpty {
+        do {
+          try await group.next()
+        } catch {
+          group.cancelAll()
+
+          throw error
+        }
+      }
+    }
+  }
+}
diff --git a/Sources/tart/Commands/Run.swift b/Sources/tart/Commands/Run.swift
index e21a7dd..b8985a2 100644
--- a/Sources/tart/Commands/Run.swift
+++ b/Sources/tart/Commands/Run.swift
@@ -489,6 +489,12 @@ struct Run: AsyncParsableCommand {
           }
         }
 
+        if #available(macOS 14, *) {
+          Task {
+            try await ControlSocket(vmDir.controlSocketURL).run()
+          }
+        }
+
         try await vm!.run()
 
         if let vncImpl = vncImpl {
diff --git a/Sources/tart/ControlSocket.swift b/Sources/tart/ControlSocket.swift
new file mode 100644
index 0000000..443a7db
--- /dev/null
+++ b/Sources/tart/ControlSocket.swift
@@ -0,0 +1,89 @@
+import Foundation
+import Network
+import os.log
+import NIO
+import NIOPosix
+
+@available(macOS 14, *)
+class ControlSocket {
+  let controlSocketURL: URL
+  let vmPort: UInt32
+  let eventLoopGroup = MultiThreadedEventLoopGroup(numberOfThreads: 1)
+  let logger: os.Logger = os.Logger(subsystem: "org.cirruslabs.tart.control-socket", category: "network")
+
+  init(_ controlSocketURL: URL, vmPort: UInt32 = 8080) {
+    self.controlSocketURL = controlSocketURL
+    self.vmPort = vmPort
+  }
+
+  func run() async throws {
+    // Remove control socket file from previous "tart run" invocations,
+    // if any, otherwise we may get the "address already in use" error
+    try? FileManager.default.removeItem(atPath: controlSocketURL.path())
+
+    let serverChannel = try await ServerBootstrap(group: eventLoopGroup)
+      .bind(unixDomainSocketPath: controlSocketURL.path()) { childChannel in
+        childChannel.eventLoop.makeCompletedFuture {
+          return try NIOAsyncChannel<ByteBuffer, ByteBuffer>(
+            wrappingChannelSynchronously: childChannel
+          )
+        }
+      }
+
+    try await withThrowingDiscardingTaskGroup { group in
+      try await serverChannel.executeThenClose { serverInbound in
+        for try await clientChannel in serverInbound {
+          group.addTask {
+            try await self.handleClient(clientChannel)
+          }
+        }
+      }
+    }
+  }
+
+  func handleClient(_ clientChannel: NIOAsyncChannel<ByteBuffer, ByteBuffer>) async throws {
+    self.logger.info("received new control socket connection from a client")
+
+    try await clientChannel.executeThenClose { clientInbound, clientOutbound in
+      self.logger.info("dialing to VM on port \(self.vmPort)...")
+
+      do {
+        guard let vmConnection = try await vm?.connect(toPort: self.vmPort) else {
+          throw RuntimeError.VMSocketFailed(self.vmPort, "VM is not running")
+        }
+
+        self.logger.info("running control socket proxy")
+
+        let vmChannel = try await ClientBootstrap(group: eventLoopGroup).withConnectedSocket(vmConnection.fileDescriptor) { childChannel in
+          childChannel.eventLoop.makeCompletedFuture {
+            try NIOAsyncChannel<ByteBuffer, ByteBuffer>(
+              wrappingChannelSynchronously: childChannel
+            )
+          }
+        }
+
+        try await vmChannel.executeThenClose { (vmInbound, vmOutbound) in
+          try await withThrowingDiscardingTaskGroup { group in
+            // Proxy data from a client (e.g. "tart exec") to a VM
+            group.addTask {
+              for try await message in clientInbound {
+                try await vmOutbound.write(message)
+              }
+            }
+
+            // Proxy data from a VM to a client (e.g. "tart exec")
+            group.addTask {
+              for try await message in vmInbound {
+                try await clientOutbound.write(message)
+              }
+            }
+          }
+        }
+
+        self.logger.info("control socket client disconnected")
+      } catch (let error) {
+        self.logger.error("control socket connection failed: \(error)")
+      }
+    }
+  }
+}
diff --git a/Sources/tart/Root.swift b/Sources/tart/Root.swift
index 3e37831..19eb87b 100644
--- a/Sources/tart/Root.swift
+++ b/Sources/tart/Root.swift
@@ -18,6 +18,7 @@ struct Root: AsyncParsableCommand {
       Login.self,
       Logout.self,
       IP.self,
+      Exec.self,
       Pull.self,
       Push.self,
       Import.self,
@@ -101,6 +102,11 @@ struct Root: AsyncParsableCommand {
         try command.run()
       }
     } catch {
+      // Not an error, just a custom exit code from "tart exec"
+      if let execCustomExitCodeError = error as? ExecCustomExitCodeError {
+        Foundation.exit(execCustomExitCodeError.exitCode)
+      }
+
       // Capture the error into Sentry
       SentrySDK.capture(error: error)
       SentrySDK.flush(timeout: 2.seconds.timeInterval)
diff --git a/Sources/tart/Term.swift b/Sources/tart/Term.swift
new file mode 100644
index 0000000..a5f1f9e
--- /dev/null
+++ b/Sources/tart/Term.swift
@@ -0,0 +1,60 @@
+import Foundation
+import System
+
+struct State {
+  fileprivate let termios: termios
+}
+
+class Term {
+  static func IsTerminal() -> Bool {
+    var termios = termios()
+
+    return tcgetattr(FileHandle.standardInput.fileDescriptor, &termios) != -1
+  }
+
+  static func MakeRaw() throws -> State {
+    var termiosOrig = termios()
+
+    var ret = tcgetattr(FileHandle.standardInput.fileDescriptor, &termiosOrig)
+    if ret == -1 {
+      let details = Errno(rawValue: CInt(errno))
+
+      throw RuntimeError.TerminalOperationFailed("failed to retrieve terminal parameters: \(details)")
+    }
+
+    var termiosRaw = termiosOrig
+    cfmakeraw(&termiosRaw)
+
+    ret = tcsetattr(FileHandle.standardInput.fileDescriptor, TCSANOW, &termiosRaw)
+    if ret == -1 {
+      let details = Errno(rawValue: CInt(errno))
+
+      throw RuntimeError.TerminalOperationFailed("failed to set terminal parameters: \(details)")
+    }
+
+    return State(termios: termiosOrig)
+  }
+
+  static func Restore(_ state: State) throws {
+    var termios = state.termios
+
+    let ret = tcsetattr(FileHandle.standardInput.fileDescriptor, TCSANOW, &termios)
+    if ret == -1 {
+      let details = Errno(rawValue: CInt(errno))
+
+      throw RuntimeError.TerminalOperationFailed("failed to set terminal parameters: \(details)")
+    }
+  }
+
+  static func GetSize() throws -> (width: UInt16, height: UInt16) {
+    var winsize = winsize()
+
+    guard ioctl(STDOUT_FILENO, TIOCGWINSZ, &winsize) != -1 else {
+      let details = Errno(rawValue: CInt(errno))
+
+      throw RuntimeError.TerminalOperationFailed("failed to get terminal size: \(details)")
+    }
+
+    return (width: winsize.ws_col, height: winsize.ws_row)
+  }
+}
diff --git a/Sources/tart/VM.swift b/Sources/tart/VM.swift
index 159b6ae..fafad8a 100644
--- a/Sources/tart/VM.swift
+++ b/Sources/tart/VM.swift
@@ -248,6 +248,19 @@ class VM: NSObject, VZVirtualMachineDelegate, ObservableObject {
     }
   }
 
+  @MainActor
+  func connect(toPort: UInt32) async throws -> VZVirtioSocketConnection {
+    guard let socketDevice = virtualMachine.socketDevices.first else {
+      throw RuntimeError.VMSocketFailed(toPort, ", VM has no socket devices configured")
+    }
+
+    guard let virtioSocketDevice = socketDevice as? VZVirtioSocketDevice else {
+      throw RuntimeError.VMSocketFailed(toPort, ", expected VM's first socket device to have a type of VZVirtioSocketDevice, got \(type(of: socketDevice)) instead")
+    }
+
+    return try await virtioSocketDevice.connect(toPort: toPort)
+  }
+
   func run() async throws {
     do {
       try await sema.waitUnlessCancelled()
@@ -409,6 +422,9 @@ class VM: NSObject, VZVirtualMachineDelegate, ObservableObject {
       configuration.consoleDevices.append(consoleDevice)
     }
 
+    // Socket device
+    configuration.socketDevices = [VZVirtioSocketDeviceConfiguration()]
+
     try configuration.validate()
 
     return configuration
diff --git a/Sources/tart/VMDirectory.swift b/Sources/tart/VMDirectory.swift
index 309e4a2..b198bb9 100644
--- a/Sources/tart/VMDirectory.swift
+++ b/Sources/tart/VMDirectory.swift
@@ -26,6 +26,9 @@ struct VMDirectory: Prunable {
   var manifestURL: URL {
     baseURL.appendingPathComponent("manifest.json")
   }
+  var controlSocketURL: URL {
+    baseURL.appendingPathComponent("control.sock")
+  }
 
   var explicitlyPulledMark: URL {
     baseURL.appendingPathComponent(".explicitly-pulled")
diff --git a/Sources/tart/VMStorageHelper.swift b/Sources/tart/VMStorageHelper.swift
index 9f26557..788e81d 100644
--- a/Sources/tart/VMStorageHelper.swift
+++ b/Sources/tart/VMStorageHelper.swift
@@ -49,6 +49,7 @@ extension Error {
 }
 
 enum RuntimeError : Error {
+  case Generic(_ message: String)
   case VMConfigurationError(_ message: String)
   case VMDoesNotExist(name: String)
   case VMMissingFiles(_ message: String)
@@ -75,6 +76,8 @@ enum RuntimeError : Error {
   case SuspendFailed(_ message: String)
   case PullFailed(_ message: String)
   case VirtualMachineLimitExceeded(_ hint: String)
+  case VMSocketFailed(_ port: UInt32, _ explanation: String)
+  case TerminalOperationFailed(_ message: String)
 }
 
 protocol HasExitCode {
@@ -84,6 +87,8 @@ protocol HasExitCode {
 extension RuntimeError : CustomStringConvertible {
   public var description: String {
     switch self {
+    case .Generic(let message):
+      return message
     case .VMConfigurationError(let message):
       return message
     case .VMDoesNotExist(let name):
@@ -136,6 +141,10 @@ extension RuntimeError : CustomStringConvertible {
       return message
     case .VirtualMachineLimitExceeded(let hint):
       return "The number of VMs exceeds the system limit\(hint)"
+    case .VMSocketFailed(let port, let explanation):
+      return "Failed to establish a VM socket connection to port \(port): \(explanation)"
+    case .TerminalOperationFailed(let message):
+      return message
     }
   }
 }