diff --git a/apps/cli-go/internal/db/diff/diff.go b/apps/cli-go/internal/db/diff/diff.go
index 05991423d6..46d465aff2 100644
--- a/apps/cli-go/internal/db/diff/diff.go
+++ b/apps/cli-go/internal/db/diff/diff.go
@@ -230,7 +230,7 @@ func migrateBaseDatabase(ctx context.Context, config pgconn.Config, migrations [
 }
 
 func diffWithStream(ctx context.Context, env []string, script string, stdout io.Writer) error {
-	cmd := []string{"edge-runtime", "start", "--main-service=."}
+	cmd := utils.EdgeRuntimeStartCmd()
 	if viper.GetBool("DEBUG") {
 		cmd = append(cmd, "--verbose")
 	}
diff --git a/apps/cli-go/internal/utils/edgeruntime.go b/apps/cli-go/internal/utils/edgeruntime.go
index 06a42b464c..d7070f3f9e 100644
--- a/apps/cli-go/internal/utils/edgeruntime.go
+++ b/apps/cli-go/internal/utils/edgeruntime.go
@@ -3,6 +3,8 @@ package utils
 import (
 	"bytes"
 	"context"
+	"fmt"
+	"net"
 	"strings"
 
 	"github.com/docker/docker/api/types/container"
@@ -11,10 +13,35 @@ import (
 	"github.com/spf13/viper"
 )
 
+// getFreeHostPort asks the OS for an unused TCP port on the host.
+func getFreeHostPort() (int, error) {
+	listener, err := net.Listen("tcp", "127.0.0.1:0")
+	if err != nil {
+		return 0, errors.Errorf("failed to allocate free port: %w", err)
+	}
+	defer listener.Close()
+	return listener.Addr().(*net.TCPAddr).Port, nil
+}
+
+// EdgeRuntimeStartCmd builds the base command for launching a one-shot Edge
+// Runtime script. The runtime's HTTP listener is bound to a free host port so
+// concurrent or leftover containers (which share the host network namespace
+// because diff containers run with NetworkMode=host) don't collide on the
+// edge-runtime default port, which surfaces as "Address already in use (os
+// error 98)". See https://github.com/supabase/cli/issues/5407.
+func EdgeRuntimeStartCmd() []string {
+	cmd := []string{"edge-runtime", "start", "--main-service=."}
+	// Skip the flag on the rare allocation failure to preserve prior behavior.
+	if port, err := getFreeHostPort(); err == nil {
+		cmd = append(cmd, fmt.Sprintf("--port=%d", port))
+	}
+	return cmd
+}
+
 // RunEdgeRuntimeScript executes a TypeScript program inside the configured Edge
 // Runtime container and streams stdout/stderr back to the caller.
 func RunEdgeRuntimeScript(ctx context.Context, env []string, script string, binds []string, errPrefix string, stdout, stderr *bytes.Buffer) error {
-	cmd := []string{"edge-runtime", "start", "--main-service=."}
+	cmd := EdgeRuntimeStartCmd()
 	if viper.GetBool("DEBUG") {
 		cmd = append(cmd, "--verbose")
 	}
diff --git a/apps/cli-go/internal/utils/edgeruntime_test.go b/apps/cli-go/internal/utils/edgeruntime_test.go
new file mode 100644
index 0000000000..8bed5b0974
--- /dev/null
+++ b/apps/cli-go/internal/utils/edgeruntime_test.go
@@ -0,0 +1,47 @@
+package utils
+
+import (
+	"strconv"
+	"strings"
+	"testing"
+
+	"github.com/stretchr/testify/assert"
+	"github.com/stretchr/testify/require"
+)
+
+func TestEdgeRuntimeStartCmd(t *testing.T) {
+	t.Run("binds an explicit free port", func(t *testing.T) {
+		cmd := EdgeRuntimeStartCmd()
+		// Base command must always be present.
+		assert.Equal(t, []string{"edge-runtime", "start", "--main-service=."}, cmd[:3])
+		// A --port flag avoids collisions on the edge-runtime default port (#5407).
+		var portFlag string
+		for _, arg := range cmd {
+			if strings.HasPrefix(arg, "--port=") {
+				portFlag = arg
+			}
+		}
+		require.NotEmpty(t, portFlag, "expected a --port flag to be set")
+		port, err := strconv.Atoi(strings.TrimPrefix(portFlag, "--port="))
+		require.NoError(t, err)
+		assert.Greater(t, port, 0)
+		assert.LessOrEqual(t, port, 65535)
+	})
+
+	t.Run("allocates a distinct port per invocation", func(t *testing.T) {
+		first := getPortArg(t, EdgeRuntimeStartCmd())
+		second := getPortArg(t, EdgeRuntimeStartCmd())
+		assert.NotEqual(t, first, second)
+	})
+}
+
+func getPortArg(t *testing.T, cmd []string) string {
+	t.Helper()
+	for _, arg := range cmd {
+		if strings.HasPrefix(arg, "--port=") {
+			return arg
+		}
+	}
+	require.FailNow(t, "missing --port flag")
+	return ""
+}