diff --git a/cli/integrationtest/controlplane_test.go b/cli/integrationtest/controlplane_test.go
index a95d4411..d652e224 100644
--- a/cli/integrationtest/controlplane_test.go
+++ b/cli/integrationtest/controlplane_test.go
@@ -483,6 +483,98 @@ timeoutSeconds: 600`, getTestConnectivityImage(t))
 	require.Equal("1234", execStdOut)
 }
 
+func TestEndToEndExecWithSocketsAndEphemeralBuffersTrickle(t *testing.T) {
+	t.Parallel()
+	skipIfEphemeralBuffersNotSupported(t)
+	require := require.New(t)
+
+	runSpec := fmt.Sprintf(`
+job:
+  codespec:
+    image: %s
+    buffers:
+      inputs: ["input"]
+      outputs: ["output"]
+    sockets:
+      - port: 9002
+        inputBuffer: input
+        outputBuffer: output
+    args:
+      - socket
+      - --port
+      - "9002"
+  buffers:
+    input: _
+    output: _
+timeoutSeconds: 600`, getTestConnectivityImage(t))
+
+	tempDir := t.TempDir()
+	runSpecPath := filepath.Join(tempDir, "runspec.yaml")
+	require.NoError(os.WriteFile(runSpecPath, []byte(runSpec), 0644))
+
+	// Create a pipe that trickles data: writes the current date every second for 10 seconds
+	pr, pw := io.Pipe()
+	inByteCount := 0
+	go func() {
+		defer pw.Close()
+		for i := range 10 {
+			n, err := fmt.Fprintf(pw, "%s\n", time.Now().Format(time.RFC3339Nano))
+			require.NoError(err)
+			inByteCount += n
+			if i < 9 {
+				time.Sleep(1 * time.Second)
+			}
+		}
+	}()
+
+	execCmd := exec.Command("tyger", "run", "exec", "--file", runSpecPath, "--log-level", "trace")
+	execCmd.Stdin = pr
+
+	stdErr := &bytes.Buffer{}
+	execCmd.Stderr = stdErr
+
+	execOutPipe, err := execCmd.StdoutPipe()
+	require.NoError(err)
+
+	require.NoError(execCmd.Start())
+
+	// Read output and record the start and stop times
+	var firstReadTime, lastReadTime time.Time
+	outByteCount := 0
+	for {
+		buf := make([]byte, 64*1024)
+		n, err := execOutPipe.Read(buf)
+		if n > 0 {
+			now := time.Now()
+			if outByteCount == 0 {
+				firstReadTime = now
+			}
+			lastReadTime = now
+			outByteCount += n
+		}
+		if err == io.EOF {
+			break
+		}
+		require.NoError(err)
+	}
+
+	execErr := execCmd.Wait()
+	t.Log(stdErr.String())
+	require.NoError(execErr)
+
+	require.Equal(inByteCount, outByteCount)
+
+	// Validate that output was received as a trickle, not all at once.
+	// The total duration between first and last received data should be at least 7 seconds.
+	totalDuration := lastReadTime.Sub(firstReadTime)
+
+	t.Logf("First output received at: %s", firstReadTime.Format(time.RFC3339Nano))
+	t.Logf("Last output received at:  %s", lastReadTime.Format(time.RFC3339Nano))
+
+	require.Greater(totalDuration.Seconds(), 5.0,
+		"Expected output to trickle over at least 5 seconds, but total duration was %s", totalDuration)
+}
+
 func TestEndToEndCreateWithShortBufferAccessTtl(t *testing.T) {
 	t.Parallel()
 	skipIfOnlyFastTests(t)
diff --git a/cli/integrationtest/testutils.go b/cli/integrationtest/testutils.go
index fb004a4d..6b6c90cd 100644
--- a/cli/integrationtest/testutils.go
+++ b/cli/integrationtest/testutils.go
@@ -12,6 +12,7 @@ import (
 	"errors"
 	"flag"
 	"fmt"
+	"io"
 	"net/http"
 	"os/exec"
 	"slices"
@@ -65,6 +66,11 @@ func (b *CmdBuilder) Stdin(stdin string) *CmdBuilder {
 	return b
 }
 
+func (b *CmdBuilder) StdinStream(stdin io.Reader) *CmdBuilder {
+	b.cmd.Stdin = stdin
+	return b
+}
+
 func (b *CmdBuilder) Run() (stdout string, stderr string, err error) {
 	defer b.cancelFunc()
 
diff --git a/cli/internal/dataplane/relayserver.go b/cli/internal/dataplane/relayserver.go
index 108459c1..2a7d537c 100644
--- a/cli/internal/dataplane/relayserver.go
+++ b/cli/internal/dataplane/relayserver.go
@@ -174,7 +174,27 @@ func RelayOutputServer(
 				}
 			}()
 
-			_, err := io.Copy(w, inputReader)
+			var err error
+			if flusher == nil {
+				_, err = io.Copy(w, inputReader)
+			} else {
+				// If the ResponseWriter supports flushing, we want to flush regularly in the case of a trickle of data.
+				buf := make([]byte, 32*1024)
+				for {
+					n, err := inputReader.Read(buf)
+					if n > 0 {
+						w.Write(buf[:n])
+						flusher.Flush()
+					}
+					if err != nil {
+						if err == io.EOF {
+							err = nil
+						}
+						break
+					}
+				}
+			}
+
 			if err != nil {
 				log.Error().Err(err).Msg("transfer failed")
 				w.Header().Set(ErrorCodeHeader, transferFailedErrorCode)