diff --git a/handler/handle_error_test.go b/handler/handle_error_test.go
new file mode 100644
index 0000000..225720c
--- /dev/null
+++ b/handler/handle_error_test.go
@@ -0,0 +1,52 @@
+package handler
+
+import (
+	"errors"
+	"io"
+	"log/slog"
+	"net/http"
+	"net/http/httptest"
+	"strings"
+	"testing"
+)
+
+func TestHandleError_WritesBodyAndHeaders(t *testing.T) {
+	cases := []struct {
+		name      string
+		debugMode bool
+		wantBody  string // substring match (http.Error appends a trailing newline)
+	}{
+		{name: "non-debug uses StatusText", debugMode: false, wantBody: http.StatusText(http.StatusInternalServerError)},
+		{name: "debug exposes error message", debugMode: true, wantBody: "boom"},
+	}
+
+	for _, tc := range cases {
+		t.Run(tc.name, func(t *testing.T) {
+			h := &Handler{
+				log:              slog.New(slog.NewTextHandler(io.Discard, nil)),
+				internalHTTPCode: http.StatusInternalServerError,
+				debugMode:        tc.debugMode,
+			}
+			rec := httptest.NewRecorder()
+
+			h.handleError(rec, errors.New("boom"))
+
+			resp := rec.Result()
+			defer func() { _ = resp.Body.Close() }()
+
+			if resp.StatusCode != http.StatusInternalServerError {
+				t.Errorf("status: got %d, want %d", resp.StatusCode, http.StatusInternalServerError)
+			}
+			if ct := resp.Header.Get("Content-Type"); !strings.HasPrefix(ct, "text/plain") {
+				t.Errorf("Content-Type: got %q, want text/plain prefix", ct)
+			}
+			if nosniff := resp.Header.Get("X-Content-Type-Options"); nosniff != "nosniff" {
+				t.Errorf("X-Content-Type-Options: got %q, want nosniff", nosniff)
+			}
+			body, _ := io.ReadAll(resp.Body)
+			if !strings.Contains(string(body), tc.wantBody) {
+				t.Errorf("body: got %q, want substring %q", body, tc.wantBody)
+			}
+		})
+	}
+}
diff --git a/handler/handler.go b/handler/handler.go
index c229a4f..429a889 100644
--- a/handler/handler.go
+++ b/handler/handler.go
@@ -4,8 +4,6 @@ import (
 	"encoding/json"
 	stderr "errors"
 	"fmt"
-	"html/template"
-	"io"
 	"log/slog"
 	"net/http"
 	"strings"
@@ -122,7 +120,15 @@ func (h *Handler) ServeHTTP(w http.ResponseWriter, r *http.Request) {
 		// marshal req.Uploads AFTER, not before, to capture the final state.
 		ups.Open(h.log, h.uploads.dir, h.uploads.forbid, h.uploads.allow)
 		if req.Uploads, err = json.Marshal(ups); err != nil {
-			h.handleRequestErr(w, r, ups, err, start)
+			// Marshaling our own Uploads struct is a server-side bug, not
+			// client input — keep the 5xx semantics rather than letting it
+			// fall through handleRequestErr's 4xx default.
+			clearUploads(h.log, r, ups)
+			h.handleError(w, err)
+			h.log.Error("marshal uploads",
+				"elapsed", time.Since(start).Milliseconds(),
+				"error", err,
+			)
 			return
 		}
 	}
@@ -247,6 +253,13 @@ func handleProtoTrailers(h map[string]*httpV2.HttpHeaderValue) {
 	delete(h, Trailer)
 }
 
+// handleRequestErr writes the response for an error produced while parsing the
+// client's request. Such errors are 4xx by construction — populateBody only
+// touches client-supplied bytes (multipart form, body, query). The default is
+// http.StatusBadRequest; call sites that know a more specific code (e.g. 413
+// for size limits) wrap the error with withStatus, which wins here via
+// errors.As. Server-internal failures must not flow through this path — see
+// handleError instead.
 func (h *Handler) handleRequestErr(w http.ResponseWriter, r *http.Request, ups *Uploads, err error, start time.Time) {
 	clearUploads(h.log, r, ups)
 
@@ -258,14 +271,9 @@ func (h *Handler) handleRequestErr(w http.ResponseWriter, r *http.Request, ups *
 		return
 	}
 
-	status := http.StatusInternalServerError
-	switch {
-	case isMaxBytesError(err):
-		status = http.StatusRequestEntityTooLarge
-	case stderr.Is(err, io.EOF), stderr.Is(err, io.ErrUnexpectedEOF):
-		status = http.StatusBadRequest
-	case stderr.Is(err, ErrMaxLevelExceeded):
-		status = http.StatusBadRequest
+	status := http.StatusBadRequest
+	if sErr, ok := stderr.AsType[*statusError](err); ok {
+		status = sErr.Status()
 	}
 
 	http.Error(w, err.Error(), status)
@@ -286,15 +294,15 @@ func (h *Handler) handleSubmitErr(w http.ResponseWriter, err error) {
 func (h *Handler) handleError(w http.ResponseWriter, err error) {
 	// internalHTTPCode is a config-provided HTTP status, defaulted to 500 and
 	// always within [100, 599] in practice. The cast is safe.
-	w.WriteHeader(int(h.internalHTTPCode)) //nolint:gosec // G115: bounded HTTP status code
+	status := int(h.internalHTTPCode) //nolint:gosec // G115: bounded HTTP status code
+	msg := http.StatusText(status)
 	if h.debugMode {
-		template.HTMLEscape(w, []byte(err.Error()))
+		msg = err.Error()
 	}
-}
-
-func isMaxBytesError(err error) bool {
-	_, ok := stderr.AsType[*http.MaxBytesError](err)
-	return ok
+	// http.Error sets Content-Type and X-Content-Type-Options: nosniff and
+	// writes msg as the body — keeps the response well-formed even when the
+	// configured internalHTTPCode is a 5xx and we're not in debug mode.
+	http.Error(w, msg, status)
 }
 
 func clearUploads(log *slog.Logger, r *http.Request, ups *Uploads) {
diff --git a/handler/request.go b/handler/request.go
index a941cf4..c5e7f7a 100644
--- a/handler/request.go
+++ b/handler/request.go
@@ -110,7 +110,7 @@ func populateBody(r *http.Request, req *httpV2.HttpHandlerRequest, uid, gid int)
 		// plugin level (plugin.applyBundledMiddleware), so gosec's
 		// "unbounded form parsing" warning is a false positive here.
 		if err := r.ParseMultipartForm(defaultMaxMemory); err != nil { //nolint:gosec // G120: bounded upstream
-			return nil, err
+			return nil, classifyParseErr(err)
 		}
 		ups, err := parseUploads(r, uid, gid)
 		if err != nil {
@@ -129,8 +129,12 @@ func populateBody(r *http.Request, req *httpV2.HttpHandlerRequest, uid, gid int)
 		return ups, nil
 
 	default:
+		// r.Body is wrapped by middleware/maxRequest.go's MaxBytesReader, so
+		// ReadAll can fail with *http.MaxBytesError on payload overflow —
+		// classifyParseErr promotes that to 413 (otherwise it would fall to
+		// handleRequestErr's 400 default).
 		var err error
 		req.Body, err = io.ReadAll(r.Body)
-		return nil, err
+		return nil, classifyParseErr(err)
 	}
 }
diff --git a/handler/status_error.go b/handler/status_error.go
new file mode 100644
index 0000000..bf91692
--- /dev/null
+++ b/handler/status_error.go
@@ -0,0 +1,41 @@
+package handler
+
+import (
+	"errors"
+	"mime/multipart"
+	"net/http"
+)
+
+// statusError carries an explicit HTTP status code through an error chain.
+// Call sites that know the correct response code wrap with withStatus;
+// handleRequestErr unwraps via errors.As so the wrapped status wins over
+// the default 4xx classification.
+type statusError struct {
+	status int
+	err    error
+}
+
+func (e *statusError) Error() string { return e.err.Error() }
+func (e *statusError) Unwrap() error { return e.err }
+func (e *statusError) Status() int   { return e.status }
+
+func withStatus(status int, err error) error {
+	if err == nil {
+		return nil
+	}
+	return &statusError{status: status, err: err}
+}
+
+// classifyParseErr promotes payload-size errors (*http.MaxBytesError and
+// multipart.ErrMessageTooLarge) to 413 by wrapping with withStatus. Other
+// errors pass through unchanged so they hit handleRequestErr's 400 default —
+// every error reaching this helper originates from parsing client input.
+func classifyParseErr(err error) error {
+	if err == nil {
+		return nil
+	}
+	if _, ok := errors.AsType[*http.MaxBytesError](err); ok || errors.Is(err, multipart.ErrMessageTooLarge) {
+		return withStatus(http.StatusRequestEntityTooLarge, err)
+	}
+	return err
+}
diff --git a/handler/status_error_test.go b/handler/status_error_test.go
new file mode 100644
index 0000000..921938a
--- /dev/null
+++ b/handler/status_error_test.go
@@ -0,0 +1,72 @@
+package handler
+
+import (
+	"errors"
+	"mime/multipart"
+	"net/http"
+	"testing"
+)
+
+func TestStatusError_Wrapping(t *testing.T) {
+	base := errors.New("boom")
+	wrapped := withStatus(http.StatusTeapot, base)
+
+	if wrapped.Error() != "boom" {
+		t.Fatalf("Error(): got %q, want %q", wrapped.Error(), "boom")
+	}
+
+	sErr, ok := errors.AsType[*statusError](wrapped)
+	if !ok {
+		t.Fatal("errors.AsType[*statusError] failed")
+	}
+	if sErr.Status() != http.StatusTeapot {
+		t.Errorf("Status(): got %d, want %d", sErr.Status(), http.StatusTeapot)
+	}
+	if !errors.Is(wrapped, base) {
+		t.Error("errors.Is should unwrap to the base error")
+	}
+}
+
+func TestStatusError_WithStatusNil(t *testing.T) {
+	if got := withStatus(http.StatusBadRequest, nil); got != nil {
+		t.Errorf("withStatus(_, nil): got %v, want nil", got)
+	}
+}
+
+func TestClassifyParseErr(t *testing.T) {
+	t.Run("nil passthrough", func(t *testing.T) {
+		if got := classifyParseErr(nil); got != nil {
+			t.Errorf("got %v, want nil", got)
+		}
+	})
+
+	t.Run("MaxBytesError promotes to 413", func(t *testing.T) {
+		err := classifyParseErr(&http.MaxBytesError{Limit: 1024})
+		sErr, ok := errors.AsType[*statusError](err)
+		if !ok || sErr.Status() != http.StatusRequestEntityTooLarge {
+			t.Errorf("got %v, want 413 wrapper", err)
+		}
+	})
+
+	t.Run("ErrMessageTooLarge promotes to 413", func(t *testing.T) {
+		err := classifyParseErr(multipart.ErrMessageTooLarge)
+		sErr, ok := errors.AsType[*statusError](err)
+		if !ok || sErr.Status() != http.StatusRequestEntityTooLarge {
+			t.Errorf("got %v, want 413 wrapper", err)
+		}
+	})
+
+	t.Run("unknown error passes through unwrapped", func(t *testing.T) {
+		// "invalid semicolon separator in query" is a plain errors.New from
+		// url.ParseQuery — by passing through (no statusError wrapper), it
+		// lands on handleRequestErr's 400 default. Protects issue #2353.
+		base := errors.New("invalid semicolon separator in query")
+		got := classifyParseErr(base)
+		if !errors.Is(got, base) {
+			t.Errorf("expected base error preserved in chain; got %v", got)
+		}
+		if _, ok := errors.AsType[*statusError](got); ok {
+			t.Error("plain errors must not be wrapped with a status")
+		}
+	})
+}
diff --git a/tests/handler_test.go b/tests/handler_test.go
index 45e866f..0728dd2 100644
--- a/tests/handler_test.go
+++ b/tests/handler_test.go
@@ -17,6 +17,7 @@ import (
 	httpV2 "github.com/roadrunner-server/api-go/v6/http/v2"
 	"github.com/roadrunner-server/http/v6/config"
 	"github.com/roadrunner-server/http/v6/handler"
+	httpMw "github.com/roadrunner-server/http/v6/middleware"
 	"github.com/roadrunner-server/http/v6/proxy"
 	"github.com/stretchr/testify/assert"
 	"github.com/stretchr/testify/require"
@@ -469,6 +470,70 @@ func TestHandler_Multipart_PATCH(t *testing.T) {
 	assertStandardFormTree(t, res, "value")
 }
 
+// TestHandler_NonMultipart_OversizeBody guards against the regression where a
+// non-multipart body exceeding MaxRequestSize returned 400 instead of 413,
+// because the original handleRequestErr's explicit MaxBytesError case had
+// been collapsed into the 400 default. classifyParseErr now promotes the
+// MaxBytesError on the io.ReadAll path back to 413.
+func TestHandler_NonMultipart_OversizeBody(t *testing.T) {
+	const maxBytes = 64
+	cfg := defaultCfg()
+	q := proxy.NewQueue(cfg.Proxy.InboxSize)
+	stop := helpers.StartFakeWorker(t.Context(), q, multipartEchoResponder)
+	t.Cleanup(stop)
+
+	h := handler.NewHandler(cfg, q, testLog.SlogLogger())
+	// Wrap with the same MaxRequestSize middleware the plugin applies in
+	// production (init.go) — without it ReadAll never sees MaxBytesError.
+	hs := &http.Server{
+		Addr:              "127.0.0.1:8190",
+		Handler:           httpMw.MaxRequestSize(h, maxBytes),
+		ReadHeaderTimeout: time.Minute,
+	}
+	go func() {
+		if err := hs.ListenAndServe(); err != nil && !errors.Is(err, http.ErrServerClosed) {
+			t.Errorf("listen: %v", err)
+		}
+	}()
+	t.Cleanup(func() { _ = hs.Shutdown(context.Background()) })
+	time.Sleep(10 * time.Millisecond)
+
+	body := strings.Repeat("x", int(maxBytes)*4)
+	req, err := http.NewRequestWithContext(t.Context(), http.MethodPost, "http://127.0.0.1:8190/", strings.NewReader(body))
+	require.NoError(t, err)
+	req.Header.Set("Content-Type", "application/json")
+
+	r, err := http.DefaultClient.Do(req)
+	require.NoError(t, err)
+	defer func() { _ = r.Body.Close() }()
+
+	assert.Equal(t, http.StatusRequestEntityTooLarge, r.StatusCode)
+}
+
+// TestHandler_Multipart_SemicolonInQuery covers issue #2353: a malformed
+// query string causes ParseMultipartForm (which internally parses the URL
+// query) to fail with "invalid semicolon separator in query". The response
+// must be 400 Bad Request, not the historical 500.
+func TestHandler_Multipart_SemicolonInQuery(t *testing.T) {
+	env := newHandlerEnv(t, "127.0.0.1:8189", defaultCfg(), multipartEchoResponder)
+	defer env.close(t)
+
+	var mb bytes.Buffer
+	w := multipart.NewWriter(&mb)
+	require.NoError(t, w.WriteField("key", "value"))
+	require.NoError(t, w.Close())
+
+	req, err := http.NewRequestWithContext(t.Context(), http.MethodPost, "http://127.0.0.1:8189/?a=b;c", &mb)
+	require.NoError(t, err)
+	req.Header.Set("Content-Type", w.FormDataContentType())
+
+	r, err := http.DefaultClient.Do(req)
+	require.NoError(t, err)
+	defer func() { _ = r.Body.Close() }()
+
+	assert.Equal(t, http.StatusBadRequest, r.StatusCode)
+}
+
 func doMultipartFormPost(t *testing.T, method, urlStr string) map[string]any {
 	t.Helper()
 	var mb bytes.Buffer
diff --git a/tests/http_plugin_test.go b/tests/http_plugin_test.go
index cefd634..abeb4f5 100644
--- a/tests/http_plugin_test.go
+++ b/tests/http_plugin_test.go
@@ -1714,7 +1714,7 @@ func TestHTTPBigRequestSize(t *testing.T) {
 	b, err := io.ReadAll(r.Body)
 	assert.NoError(t, err)
 	assert.Equal(t, http.StatusRequestEntityTooLarge, r.StatusCode)
-	assert.Equal(t, "serve_http: http: request body too large\n", string(b))
+	assert.Equal(t, "http: request body too large\n", string(b))
 
 	err = r.Body.Close()
 	assert.NoError(t, err)