diff --git a/changelog/14328.txt b/changelog/14328.txt
new file mode 100644
index 0000000000000..c5e45f0a30c83
--- /dev/null
+++ b/changelog/14328.txt
@@ -0,0 +1,3 @@
+```release-note:change
+core: A request that fails path validation due to relative path check will now be responded to with a 400 rather than 500.
+```
diff --git a/http/logical_test.go b/http/logical_test.go
index 05d6bf4eacd4d..7d79553b19f9d 100644
--- a/http/logical_test.go
+++ b/http/logical_test.go
@@ -14,6 +14,8 @@ import (
 	"testing"
 	"time"
 
+	"github.com/hashicorp/vault/api"
+	credUserpass "github.com/hashicorp/vault/builtin/credential/userpass"
 	"github.com/hashicorp/vault/internalshared/configutil"
 	"github.com/hashicorp/vault/sdk/helper/consts"
 	"github.com/hashicorp/vault/sdk/helper/logging"
@@ -499,3 +501,75 @@ func TestLogical_ShouldParseForm(t *testing.T) {
 		}
 	}
 }
+
+func TestLogical_ErrRelativePath(t *testing.T) {
+	coreConfig := &vault.CoreConfig{
+		CredentialBackends: map[string]logical.Factory{
+			"userpass": credUserpass.Factory,
+		},
+	}
+
+	cluster := vault.NewTestCluster(t, coreConfig, &vault.TestClusterOptions{
+		HandlerFunc: Handler,
+	})
+
+	cluster.Start()
+	defer cluster.Cleanup()
+
+	cores := cluster.Cores
+
+	core := cores[0].Core
+	c := cluster.Cores[0].Client
+	vault.TestWaitActive(t, core)
+
+	err := c.Sys().EnableAuthWithOptions("userpass", &api.EnableAuthOptions{
+		Type: "userpass",
+	})
+	if err != nil {
+		t.Fatalf("failed to enable userpass, err: %v", err)
+	}
+
+	resp, err := c.Logical().Read("auth/userpass/users/user..aaa")
+
+	if err == nil || resp != nil {
+		t.Fatalf("expected read request to fail, resp: %#v, err: %v", resp, err)
+	}
+
+	respErr, ok := err.(*api.ResponseError)
+
+	if !ok {
+		t.Fatalf("unexpected error type, err: %#v", err)
+	}
+
+	if respErr.StatusCode != 400 {
+		t.Errorf("expected 400 response for read, actual: %d", respErr.StatusCode)
+	}
+
+	if !strings.Contains(respErr.Error(), logical.ErrRelativePath.Error()) {
+		t.Errorf("expected response for read to include %q", logical.ErrRelativePath.Error())
+	}
+
+	data := map[string]interface{}{
+		"password": "abc123",
+	}
+
+	resp, err = c.Logical().Write("auth/userpass/users/user..aaa", data)
+
+	if err == nil || resp != nil {
+		t.Fatalf("expected write request to fail, resp: %#v, err: %v", resp, err)
+	}
+
+	respErr, ok = err.(*api.ResponseError)
+
+	if !ok {
+		t.Fatalf("unexpected error type, err: %#v", err)
+	}
+
+	if respErr.StatusCode != 400 {
+		t.Errorf("expected 400 response for write, actual: %d", respErr.StatusCode)
+	}
+
+	if !strings.Contains(respErr.Error(), logical.ErrRelativePath.Error()) {
+		t.Errorf("expected response for write to include %q", logical.ErrRelativePath.Error())
+	}
+}
diff --git a/sdk/logical/response_util.go b/sdk/logical/response_util.go
index a05f74684951e..83a5fac44808e 100644
--- a/sdk/logical/response_util.go
+++ b/sdk/logical/response_util.go
@@ -118,6 +118,8 @@ func RespondErrorCommon(req *Request, resp *Response, err error) (int, error) {
 			statusCode = http.StatusTooManyRequests
 		case errwrap.Contains(err, ErrMissingRequiredState.Error()):
 			statusCode = http.StatusPreconditionFailed
+		case errwrap.Contains(err, ErrRelativePath.Error()):
+			statusCode = http.StatusBadRequest
 		}
 	}
 
diff --git a/vault/request_handling.go b/vault/request_handling.go
index ebccff6f3f9f8..f39ccbbdca4ce 100644
--- a/vault/request_handling.go
+++ b/vault/request_handling.go
@@ -299,6 +299,8 @@ func (c *Core) checkToken(ctx context.Context, req *logical.Request, unauth bool
 		case logical.ErrUnsupportedPath:
 			// fail later via bad path to avoid confusing items in the log
 			checkExists = false
+		case logical.ErrRelativePath:
+			return nil, te, errutil.UserError{Err: err.Error()}
 		case nil:
 			if existsResp != nil && existsResp.IsError() {
 				return nil, te, existsResp.Error()
@@ -752,6 +754,9 @@ func (c *Core) handleRequest(ctx context.Context, req *logical.Request) (retResp
 
 	// Validate the token
 	auth, te, ctErr := c.checkToken(ctx, req, false)
+	if ctErr == logical.ErrRelativePath {
+		return logical.ErrorResponse(ctErr.Error()), nil, ctErr
+	}
 	if ctErr == logical.ErrPerfStandbyPleaseForward {
 		return nil, nil, ctErr
 	}