diff --git a/api/event_stream.go b/api/event_stream.go
index f2a1bc79002..49a666709b1 100644
--- a/api/event_stream.go
+++ b/api/event_stream.go
@@ -167,6 +167,8 @@ func (c *Client) EventStream() *EventStream {
 
 // Stream establishes a new subscription to Nomad's event stream and streams
 // results back to the returned channel.
+//
+// Events stop being emitted once the Events.Err field is non-nil.
 func (e *EventStream) Stream(ctx context.Context, topics map[Topic][]string, index uint64, q *QueryOptions) (<-chan *Events, error) {
 	r, err := e.client.newRequest("GET", "/v1/event/stream")
 	if err != nil {
@@ -220,6 +222,11 @@ func (e *EventStream) Stream(ctx context.Context, topics map[Topic][]string, ind
 				return
 			case eventsCh <- &events:
 			}
+
+			// There are no recoverable Decode errors, so return on error.
+			if events.Err != nil {
+				return
+			}
 		}
 	}()
 
diff --git a/api/event_stream_test.go b/api/event_stream_test.go
index 0e701b8fc52..b4455fa8309 100644
--- a/api/event_stream_test.go
+++ b/api/event_stream_test.go
@@ -6,6 +6,7 @@ package api
 import (
 	"context"
 	"encoding/json"
+	"strings"
 	"testing"
 	"time"
 
@@ -118,6 +119,42 @@ func TestEvent_Stream(t *testing.T) {
 	case <-time.After(5 * time.Second):
 		must.Unreachable(t, must.Sprint("failed waiting for event stream event"))
 	}
+
+	// Stop the server to ensure EOF is returned
+	s.Stop()
+
+	for {
+		select {
+		case event, ok := <-streamCh:
+			if !ok {
+				must.Unreachable(t, must.Sprintf("chan closed before EOF received"))
+			}
+
+			// Sadly decode doesn't return io.EOF
+			if event.Err != nil && strings.HasSuffix(event.Err.Error(), "EOF") {
+				// Succcess! Make sure chan gets closed
+				select {
+				case _, ok := <-streamCh:
+					if ok {
+						must.Unreachable(t, must.Sprintf("expected chan to close after EOF"))
+					}
+
+					// Success!
+					return
+				case <-time.After(5 * time.Second):
+					must.Unreachable(t, must.Sprint("failed waiting for event stream to close"))
+				}
+			}
+
+			if event.Err != nil {
+				must.Unreachable(t, must.Sprintf("unexpected %v (%T)", event.Err, event.Err))
+			}
+			must.Len(t, 1, event.Events)
+			must.Eq(t, "Evaluation", string(event.Events[0].Topic))
+		case <-time.After(5 * time.Second):
+			must.Unreachable(t, must.Sprint("failed waiting for event stream EOF"))
+		}
+	}
 }
 
 func TestEvent_Stream_Err_InvalidQueryParam(t *testing.T) {
diff --git a/api/internal/testutil/server.go b/api/internal/testutil/server.go
index 59799326df1..fb16ccd022a 100644
--- a/api/internal/testutil/server.go
+++ b/api/internal/testutil/server.go
@@ -143,6 +143,7 @@ type TestServer struct {
 	cmd    *exec.Cmd
 	Config *TestServerConfig
 	t      testing.TB
+	exited bool
 
 	HTTPAddr   string
 	SerfAddr   string
@@ -240,6 +241,12 @@ func NewTestServer(t testing.TB, cb ServerConfigCallback) *TestServer {
 // Stop stops the test Nomad server, and removes the Nomad data
 // directory once we are done.
 func (s *TestServer) Stop() {
+	if s.exited {
+		// Allow calling multiple times to allow for tests that use defer s.Stop()
+		// as well as stop the server during the test to assert behavior.
+		return
+	}
+
 	s.t.Cleanup(func() {
 		_ = os.RemoveAll(s.Config.DataDir)
 	})
@@ -258,6 +265,7 @@ func (s *TestServer) Stop() {
 
 	select {
 	case <-done:
+		s.exited = true
 		return
 	case <-time.After(5 * time.Second):
 		s.t.Logf("timed out waiting for process to gracefully terminate")
@@ -268,6 +276,7 @@ func (s *TestServer) Stop() {
 
 	select {
 	case <-done:
+		s.exited = true
 	case <-time.After(5 * time.Second):
 		s.t.Logf("timed out waiting for process to be killed")
 	}