diff --git a/cmd/runner/runner.go b/cmd/runner/runner.go
index 72424c1b6..e620b53b3 100644
--- a/cmd/runner/runner.go
+++ b/cmd/runner/runner.go
@@ -15,7 +15,12 @@ type runnerOpts struct {
 	r running
 }
 
-func NewCommand(config *settings.Config, preRunE validator.Validator) *cobra.Command {
+func NewCommand(rootConfig *settings.Config, preRunE validator.Validator) *cobra.Command {
+	// The runner API versioning is decoupled from the other Circle APIs. Here we make a copy of the root configuration,
+	// and update the rest endpoint accordingly
+	config := *rootConfig
+	config.RestEndpoint = "/api/v3"
+
 	var opts runnerOpts
 	cmd := &cobra.Command{
 		Use:   "runner",
@@ -27,7 +32,7 @@ func NewCommand(config *settings.Config, preRunE validator.Validator) *cobra.Com
 			} else {
 				host = config.Host
 			}
-			opts.r = runner.New(rest.NewFromConfig(host, config))
+			opts.r = runner.New(rest.NewFromConfig(host, &config))
 		},
 	}
 
diff --git a/cmd/runner/runner_test.go b/cmd/runner/runner_test.go
new file mode 100644
index 000000000..cfef51286
--- /dev/null
+++ b/cmd/runner/runner_test.go
@@ -0,0 +1,31 @@
+package runner
+
+import (
+	"net/http"
+	"net/http/httptest"
+	"testing"
+
+	"gotest.tools/v3/assert"
+	"gotest.tools/v3/assert/cmp"
+
+	"github.com/CircleCI-Public/circleci-cli/settings"
+)
+
+func Test_NewCommand(t *testing.T) {
+	t.Run("Runner uses /api/v3", func(t *testing.T) {
+		server := httptest.NewServer(http.HandlerFunc(func(w http.ResponseWriter, r *http.Request) {
+			assert.Check(t, cmp.Equal(r.URL.EscapedPath(), "/api/v3/runner"))
+
+			w.Header().Set("Content-Type", "application/json")
+			_, err := w.Write([]byte(`{"items":[]}`))
+			assert.NilError(t, err)
+			w.WriteHeader(http.StatusOK)
+		}))
+		t.Cleanup(server.Close)
+
+		cmd := NewCommand(&settings.Config{Host: server.URL, HTTPClient: &http.Client{}}, nil)
+		cmd.SetArgs([]string{"instance", "ls", "my-namespace"})
+		err := cmd.Execute()
+		assert.NilError(t, err)
+	})
+}