diff --git a/go/cmd/vtctldclient/command/keyspace_routing_rules.go b/go/cmd/vtctldclient/command/keyspace_routing_rules.go
index 7d1134d3abf..68aaa35b8bb 100644
--- a/go/cmd/vtctldclient/command/keyspace_routing_rules.go
+++ b/go/cmd/vtctldclient/command/keyspace_routing_rules.go
@@ -82,7 +82,7 @@ func commandApplyKeyspaceRoutingRules(cmd *cobra.Command, args []string) error {
 	}
 
 	krr := &vschemapb.KeyspaceRoutingRules{}
-	if err := json2.Unmarshal(rulesBytes, &krr); err != nil {
+	if err := json2.UnmarshalPB(rulesBytes, krr); err != nil {
 		return err
 	}
 
diff --git a/go/cmd/vtctldclient/command/routing_rules.go b/go/cmd/vtctldclient/command/routing_rules.go
index 0ffee0c2c24..8a228589098 100644
--- a/go/cmd/vtctldclient/command/routing_rules.go
+++ b/go/cmd/vtctldclient/command/routing_rules.go
@@ -82,7 +82,7 @@ func commandApplyRoutingRules(cmd *cobra.Command, args []string) error {
 	}
 
 	rr := &vschemapb.RoutingRules{}
-	if err := json2.Unmarshal(rulesBytes, &rr); err != nil {
+	if err := json2.UnmarshalPB(rulesBytes, rr); err != nil {
 		return err
 	}
 
diff --git a/go/cmd/vtctldclient/command/shard_routing_rules.go b/go/cmd/vtctldclient/command/shard_routing_rules.go
index 10ce7e81747..2214269d0f3 100644
--- a/go/cmd/vtctldclient/command/shard_routing_rules.go
+++ b/go/cmd/vtctldclient/command/shard_routing_rules.go
@@ -87,7 +87,7 @@ func commandApplyShardRoutingRules(cmd *cobra.Command, args []string) error {
 	}
 
 	srr := &vschemapb.ShardRoutingRules{}
-	if err := json2.Unmarshal(rulesBytes, &srr); err != nil {
+	if err := json2.UnmarshalPB(rulesBytes, srr); err != nil {
 		return err
 	}
 	// Round-trip so when we display the result it's readable.
diff --git a/go/json2/unmarshal.go b/go/json2/unmarshal.go
index e382b8ad47a..e2034fa71c9 100644
--- a/go/json2/unmarshal.go
+++ b/go/json2/unmarshal.go
@@ -33,8 +33,7 @@ var carriageReturn = []byte("\n")
 // efficient and should not be used for high QPS operations.
 func Unmarshal(data []byte, v any) error {
 	if pb, ok := v.(proto.Message); ok {
-		opts := protojson.UnmarshalOptions{DiscardUnknown: true}
-		return annotate(data, opts.Unmarshal(data, pb))
+		return UnmarshalPB(data, pb)
 	}
 	return annotate(data, json.Unmarshal(data, v))
 }
@@ -53,3 +52,9 @@ func annotate(data []byte, err error) error {
 
 	return fmt.Errorf("line: %d, position %d: %v", line, pos, err)
 }
+
+// UnmarshalPB is similar to Unmarshal but specifically for proto.Message to add type safety.
+func UnmarshalPB(data []byte, pb proto.Message) error {
+	opts := protojson.UnmarshalOptions{DiscardUnknown: true}
+	return annotate(data, opts.Unmarshal(data, pb))
+}
diff --git a/go/json2/unmarshal_test.go b/go/json2/unmarshal_test.go
index ff18a29def8..1ba3368d5ca 100644
--- a/go/json2/unmarshal_test.go
+++ b/go/json2/unmarshal_test.go
@@ -91,3 +91,14 @@ func TestAnnotate(t *testing.T) {
 		require.Equal(t, tcase.err, err, "annotate(%s, %v) error", string(tcase.data), tcase.err)
 	}
 }
+
+func TestUnmarshalPB(t *testing.T) {
+	want := &emptypb.Empty{}
+	json, err := protojson.Marshal(want)
+	require.NoError(t, err)
+
+	var got emptypb.Empty
+	err = UnmarshalPB(json, &got)
+	require.NoError(t, err)
+	require.Equal(t, want, &got)
+}
diff --git a/go/test/endtoend/vreplication/vreplication_vtctldclient_cli_test.go b/go/test/endtoend/vreplication/vreplication_vtctldclient_cli_test.go
index bca51512a3c..4a3f16a1cc9 100644
--- a/go/test/endtoend/vreplication/vreplication_vtctldclient_cli_test.go
+++ b/go/test/endtoend/vreplication/vreplication_vtctldclient_cli_test.go
@@ -19,6 +19,7 @@ package vreplication
 import (
 	"encoding/json"
 	"fmt"
+	"os"
 	"slices"
 	"strings"
 	"testing"
@@ -27,6 +28,7 @@ import (
 	"golang.org/x/exp/maps"
 	"google.golang.org/protobuf/encoding/protojson"
 
+	"vitess.io/vitess/go/json2"
 	"vitess.io/vitess/go/test/endtoend/cluster"
 
 	binlogdatapb "vitess.io/vitess/go/vt/proto/binlogdata"
@@ -61,6 +63,9 @@ func TestVtctldclientCLI(t *testing.T) {
 	workflowName := "wf1"
 	targetTabs := setupMinimalCustomerKeyspace(t)
 
+	t.Run("RoutingRulesApply", func(t *testing.T) {
+		testRoutingRulesApplyCommands(t)
+	})
 	t.Run("WorkflowList", func(t *testing.T) {
 		testWorkflowList(t, sourceKeyspaceName, targetKeyspaceName)
 	})
@@ -438,3 +443,138 @@ func validateMoveTablesWorkflow(t *testing.T, workflows []*vtctldatapb.Workflow)
 	require.Equal(t, binlogdatapb.OnDDLAction_STOP, bls.OnDdl)
 	require.True(t, bls.StopAfterCopy)
 }
+
+// Test that routing rules can be applied using the vtctldclient CLI for all types of routing rules.
+func testRoutingRulesApplyCommands(t *testing.T) {
+	var rulesBytes []byte
+	var err error
+	var validateRules func(want, got string)
+
+	ruleTypes := []string{"RoutingRules", "ShardRoutingRules", "KeyspaceRoutingRules"}
+	for _, typ := range ruleTypes {
+		switch typ {
+		case "RoutingRules":
+			rr := &vschemapb.RoutingRules{
+				Rules: []*vschemapb.RoutingRule{
+					{
+						FromTable: "from1",
+						ToTables:  []string{"to1", "to2"},
+					},
+				},
+			}
+			rulesBytes, err = json2.MarshalPB(rr)
+			require.NoError(t, err)
+			validateRules = func(want, got string) {
+				var wantRules = &vschemapb.RoutingRules{}
+				require.NoError(t, json2.UnmarshalPB([]byte(want), wantRules))
+				var gotRules = &vschemapb.RoutingRules{}
+				require.NoError(t, json2.UnmarshalPB([]byte(got), gotRules))
+				require.EqualValues(t, wantRules, gotRules)
+			}
+		case "ShardRoutingRules":
+			srr := &vschemapb.ShardRoutingRules{
+				Rules: []*vschemapb.ShardRoutingRule{
+					{
+						FromKeyspace: "from1",
+						ToKeyspace:   "to1",
+						Shard:        "-80",
+					},
+				},
+			}
+			rulesBytes, err = json2.MarshalPB(srr)
+			require.NoError(t, err)
+			validateRules = func(want, got string) {
+				var wantRules = &vschemapb.ShardRoutingRules{}
+				require.NoError(t, json2.UnmarshalPB([]byte(want), wantRules))
+				var gotRules = &vschemapb.ShardRoutingRules{}
+				require.NoError(t, json2.UnmarshalPB([]byte(got), gotRules))
+				require.EqualValues(t, wantRules, gotRules)
+			}
+		case "KeyspaceRoutingRules":
+			krr := &vschemapb.KeyspaceRoutingRules{
+				Rules: []*vschemapb.KeyspaceRoutingRule{
+					{
+						FromKeyspace: "from1",
+						ToKeyspace:   "to1",
+					},
+				},
+			}
+			rulesBytes, err = json2.MarshalPB(krr)
+			require.NoError(t, err)
+			validateRules = func(want, got string) {
+				var wantRules = &vschemapb.KeyspaceRoutingRules{}
+				require.NoError(t, json2.UnmarshalPB([]byte(want), wantRules))
+				var gotRules = &vschemapb.KeyspaceRoutingRules{}
+				require.NoError(t, json2.UnmarshalPB([]byte(got), gotRules))
+				require.EqualValues(t, wantRules, gotRules)
+			}
+		default:
+			require.FailNow(t, "Unknown type %s", typ)
+		}
+		testOneRoutingRulesCommand(t, typ, string(rulesBytes), validateRules)
+	}
+
+}
+
+// For a given routing rules type, test that the rules can be applied using the vtctldclient CLI.
+// We test both inline and file-based rules.
+// The test also validates that both camelCase and snake_case key names work correctly.
+func testOneRoutingRulesCommand(t *testing.T, typ string, rules string, validateRules func(want, got string)) {
+	type routingRulesTest struct {
+		name    string
+		rules   string
+		useFile bool // if true, use a file to pass the rules
+	}
+	tests := []routingRulesTest{
+		{
+			name:  "inline",
+			rules: rules,
+		},
+		{
+			name:    "file",
+			rules:   rules,
+			useFile: true,
+		},
+		{
+			name:  "empty", // finally, cleanup rules
+			rules: "{}",
+		},
+	}
+	for _, tt := range tests {
+		t.Run(typ+"/"+tt.name, func(t *testing.T) {
+			wantRules := tt.rules
+			// The input rules are in camelCase, since they are the output of json2.MarshalPB
+			// The first iteration uses the output of routing rule Gets which are in snake_case.
+			for _, keyCase := range []string{"camelCase", "snake_case"} {
+				t.Run(keyCase, func(t *testing.T) {
+					var args []string
+					apply := fmt.Sprintf("Apply%s", typ)
+					get := fmt.Sprintf("Get%s", typ)
+					args = append(args, apply)
+					if tt.useFile {
+						tmpFile, err := os.CreateTemp("", fmt.Sprintf("%s_rules.json", tt.name))
+						require.NoError(t, err)
+						defer os.Remove(tmpFile.Name())
+						_, err = tmpFile.WriteString(wantRules)
+						require.NoError(t, err)
+						args = append(args, "--rules-file", tmpFile.Name())
+					} else {
+						args = append(args, "--rules", wantRules)
+					}
+					var output string
+					var err error
+					if output, err = vc.VtctldClient.ExecuteCommandWithOutput(args...); err != nil {
+						require.FailNowf(t, "failed action", apply, "%v: %s", err, output)
+					}
+					if output, err = vc.VtctldClient.ExecuteCommandWithOutput(get); err != nil {
+						require.FailNowf(t, "failed action", get, "%v: %s", err, output)
+					}
+					validateRules(wantRules, output)
+					// output of GetRoutingRules is in snake_case and we use it for the next iteration which
+					// tests applying rules with snake_case keys.
+					wantRules = output
+				})
+			}
+		})
+	}
+}