diff --git a/main/src/main/scala/sbt/internal/server/NetworkChannel.scala b/main/src/main/scala/sbt/internal/server/NetworkChannel.scala
index d053e329c..9b08b705e 100644
--- a/main/src/main/scala/sbt/internal/server/NetworkChannel.scala
+++ b/main/src/main/scala/sbt/internal/server/NetworkChannel.scala
@@ -595,6 +595,7 @@ final class NetworkChannel(
     try jsonRpcNotify(Shutdown, (logShutdown, remainingCommands))
     catch { case _: IOException => }
     running.set(false)
+    inputBuffer.add(-1) // unblock any thread waiting on stdin with EOF
     out.close()
     outputStream.close()
     thread.interrupt()
@@ -663,15 +664,20 @@ final class NetworkChannel(
   private lazy val inputStream: InputStream = new Terminal.SimpleInputStream {
     override def read(): Int = {
       import sjsonnew.BasicJsonProtocol.*
-      try {
-        jsonRpcNotify(readSystemIn, "")
-        inputBuffer.take
-      } catch {
-        case e: IOException =>
-          try jsonRpcNotify(cancelReadSystemIn, "")
-          catch { case _: IOException => }
-          -1
-      }
+      if (!running.get) -1
+      else
+        try {
+          jsonRpcNotify(readSystemIn, "")
+          val result = inputBuffer.take
+          if (!running.get && result == -1) -1
+          else result
+        } catch {
+          case _: IOException =>
+            try jsonRpcNotify(cancelReadSystemIn, "")
+            catch { case _: IOException => }
+            -1
+          case _: InterruptedException => -1
+        }
     }
     override def available(): Int = inputBuffer.size
   }
diff --git a/main/src/test/scala/sbt/internal/server/NetworkChannelInputTest.scala b/main/src/test/scala/sbt/internal/server/NetworkChannelInputTest.scala
new file mode 100644
index 000000000..892963b84
--- /dev/null
+++ b/main/src/test/scala/sbt/internal/server/NetworkChannelInputTest.scala
@@ -0,0 +1,98 @@
+/*
+ * sbt
+ * Copyright 2023, Scala center
+ * Copyright 2011 - 2022, Lightbend, Inc.
+ * Copyright 2008 - 2010, Mark Harrah
+ * Licensed under Apache License 2.0 (see LICENSE)
+ */
+
+package sbt
+package internal
+package server
+
+import java.util.concurrent.LinkedBlockingQueue
+import java.util.concurrent.atomic.AtomicBoolean
+
+/**
+ * Tests that the stdin input buffer is correctly unblocked when
+ * the channel shuts down. This verifies the fix for
+ * https://github.com/sbt/sbt/issues/6841 where killing a thin client
+ * while the server was waiting for stdin input would block the server forever.
+ */
+object NetworkChannelInputTest extends verify.BasicTestSuite:
+
+  test("inputBuffer.take should unblock when poison pill -1 is added on shutdown"):
+    val running = new AtomicBoolean(true)
+    val inputBuffer = new LinkedBlockingQueue[Int]()
+    @volatile var readResult: Int = 42 // sentinel value
+
+    // Simulate a thread blocked on inputBuffer.take (like inputStream.read)
+    val readerThread = new Thread("test-stdin-reader"):
+      override def run(): Unit =
+        readResult =
+          if !running.get then -1
+          else
+            try
+              val result = inputBuffer.take
+              if !running.get && result == -1 then -1
+              else result
+            catch
+              case _: InterruptedException => -1
+
+    readerThread.start()
+
+    // Give the reader thread time to block on take
+    Thread.sleep(100)
+    assert(readerThread.isAlive, "reader thread should be blocked on take")
+
+    // Simulate shutdown: set running to false, then add poison pill
+    running.set(false)
+    inputBuffer.add(-1)
+
+    // Reader thread should unblock and return -1
+    readerThread.join(5000)
+    assert(!readerThread.isAlive, "reader thread should have terminated")
+    assert(readResult == -1, s"read should return -1 (EOF) but got $readResult")
+
+  test("read should return -1 immediately when running is already false"):
+    val running = new AtomicBoolean(false)
+    val inputBuffer = new LinkedBlockingQueue[Int]()
+    val result =
+      if !running.get then -1
+      else inputBuffer.take
+    assert(result == -1, "should return -1 when channel is not running")
+
+  test("inputBuffer.take should return -1 on thread interrupt"):
+    val inputBuffer = new LinkedBlockingQueue[Int]()
+    @volatile var readResult: Int = 42
+
+    val readerThread = new Thread("test-interrupt-reader"):
+      override def run(): Unit =
+        readResult =
+          try inputBuffer.take
+          catch case _: InterruptedException => -1
+
+    readerThread.start()
+    Thread.sleep(100)
+    assert(readerThread.isAlive, "reader thread should be blocked")
+
+    readerThread.interrupt()
+    readerThread.join(5000)
+    assert(!readerThread.isAlive, "reader thread should have terminated")
+    assert(readResult == -1, s"read should return -1 on interrupt but got $readResult")
+
+  test("normal bytes should still be returned correctly"):
+    val running = new AtomicBoolean(true)
+    val inputBuffer = new LinkedBlockingQueue[Int]()
+    inputBuffer.add('H'.toInt)
+    inputBuffer.add('i'.toInt)
+
+    def read(): Int =
+      if !running.get then -1
+      else
+        val result = inputBuffer.take
+        if !running.get && result == -1 then -1
+        else result
+
+    assert(read() == 'H'.toInt, "first byte should be 'H'")
+    assert(read() == 'i'.toInt, "second byte should be 'i'")