diff --git a/components/AccountSettings.tsx b/components/AccountSettings.tsx
index 8055898..a4ddde7 100644
--- a/components/AccountSettings.tsx
+++ b/components/AccountSettings.tsx
@@ -4,13 +4,11 @@ import { useI18n } from "@/components/I18nProvider";
 import { useState } from "react";
 import { useRouter } from "next/navigation";
 import { UserRound, LockKeyhole, Mail } from "lucide-react";
-import { createBrowserClient } from "@supabase/ssr";
 import { api } from "./StartGame";
 import { PasswordForm } from "./PasswordForm";
 import { displayNameSchema } from "@/shared/account";
 import {
   defaultGlowColor,
-  profileAvatarBucket,
   profileAvatarMaxBytes,
   profileAvatarMimeTypes,
   type ProfileAppearance,
@@ -68,37 +66,18 @@ export function AccountSettings({
       setPhotoError("Choose a JPG, PNG or WebP image.");
       return;
     }
-    const extension =
-      file.type === "image/jpeg"
-        ? "jpg"
-        : file.type === "image/png"
-          ? "png"
-          : "webp";
-    const path = `${accountId}/${crypto.randomUUID()}.${extension}`;
-    const client = createBrowserClient(
-      process.env.NEXT_PUBLIC_SUPABASE_URL!,
-      process.env.NEXT_PUBLIC_SUPABASE_PUBLISHABLE_KEY!,
-    );
     setPhotoBusy(true);
-    let uploaded = false;
     try {
-      const { error: uploadError } = await client.storage
-        .from(profileAvatarBucket)
-        .upload(path, file, {
-          cacheControl: "31536000",
-          contentType: file.type,
-          upsert: false,
-        });
-      if (uploadError)
-        throw new Error("Could not upload your profile photo. Please try again.");
-      uploaded = true;
-      await api("profile", { avatarPath: path }, "PATCH");
-      setPhotoPath(path);
+      const form = new FormData();
+      form.append("photo", file);
+      const result = await api<{ profile: { avatar_path: string } }>(
+        "profile/avatar",
+        form,
+      );
+      setPhotoPath(result.profile.avatar_path);
       setPhotoSaved(true);
       router.refresh();
     } catch (error) {
-      if (uploaded)
-        await client.storage.from(profileAvatarBucket).remove([path]);
       setPhotoError((error as Error).message);
     } finally {
       setPhotoBusy(false);
diff --git a/lib/account-api.ts b/lib/account-api.ts
index 9797a79..3d92be3 100644
--- a/lib/account-api.ts
+++ b/lib/account-api.ts
@@ -1,5 +1,7 @@
 import "server-only";
 import { createClient } from "@supabase/supabase-js";
+import { randomUUID } from "node:crypto";
+import sharp from "sharp";
 import { NextRequest, NextResponse } from "next/server";
 import {
   admin,
@@ -10,6 +12,8 @@ import {
   accountState,
 } from "./supabase";
 import { accountProfile } from "./profile";
+import { browserAccount } from "./request-security";
+import { ServiceError } from "./service-error";
 import {
   authActionSchema,
   authDestination,
@@ -24,7 +28,6 @@ import { issueInitialPassword } from "@/shared/initial-password";
 import {
   profileAvatarBucket,
   profileAvatarMaxBytes,
-  profileAvatarMimeTypes,
 } from "@/shared/profile-appearance";
 
 type Context = {
@@ -33,6 +36,98 @@ type Context = {
 };
 const json = (body: unknown, status = 200) =>
   NextResponse.json(body, { status, headers: { "Cache-Control": "no-store" } });
+const avatarRequestLimit = profileAvatarMaxBytes + 64 * 1024;
+
+async function avatarFile(request: NextRequest): Promise<File> {
+  const contentType = request.headers.get("content-type") ?? "";
+  if (!/^multipart\/form-data\s*;.*\bboundary=/i.test(contentType))
+    throw new ServiceError("Choose a valid profile photo", 400);
+  const contentLength = request.headers.get("content-length");
+  if (
+    contentLength &&
+    /^\d+$/.test(contentLength) &&
+    Number(contentLength) > avatarRequestLimit
+  )
+    throw new ServiceError("Image must be 5 MB or smaller", 413);
+
+  const reader = request.body?.getReader();
+  if (!reader) throw new ServiceError("Choose a profile photo", 400);
+  const chunks: Uint8Array[] = [];
+  let size = 0;
+  while (true) {
+    const { done, value } = await reader.read();
+    if (done) break;
+    size += value.byteLength;
+    if (size > avatarRequestLimit) {
+      try {
+        await reader.cancel();
+      } catch {
+        // The request is already being rejected; cancellation is best effort.
+      }
+      throw new ServiceError("Image must be 5 MB or smaller", 413);
+    }
+    chunks.push(value);
+  }
+
+  let form: FormData;
+  try {
+    const boundedRequest = new Request(request.url, {
+      method: "POST",
+      headers: { "content-type": contentType },
+      body: Buffer.concat(chunks, size),
+    });
+    form = await boundedRequest.formData();
+  } catch {
+    throw new ServiceError("Choose a valid profile photo", 400);
+  }
+  const entries = [...form.entries()];
+  if (entries.length !== 1)
+    throw new ServiceError("Choose a valid profile photo", 400);
+  const entry = entries[0]!;
+  if (
+    entry[0] !== "photo" ||
+    typeof entry[1] === "string" ||
+    !(entry[1] instanceof File)
+  )
+    throw new ServiceError("Choose a valid profile photo", 400);
+  const file = entry[1];
+  if (!file.size || file.size > profileAvatarMaxBytes)
+    throw new ServiceError("Image must be 5 MB or smaller", 413);
+  return file;
+}
+
+async function normalizedAvatar(file: File) {
+  try {
+    const image = sharp(Buffer.from(await file.arrayBuffer()), {
+      limitInputPixels: 24_000_000,
+      failOn: "error",
+      animated: false,
+    });
+    const metadata = await image.metadata();
+    if (
+      !["jpeg", "png", "webp"].includes(metadata.format ?? "") ||
+      (metadata.pages ?? 1) !== 1
+    )
+      throw new ServiceError("Choose a JPG, PNG or WebP image", 400);
+    const output = await image
+      .rotate()
+      .resize({
+        width: 512,
+        height: 512,
+        fit: "inside",
+        withoutEnlargement: true,
+      })
+      .webp({ quality: 85 })
+      .toBuffer();
+    if (output.byteLength > profileAvatarMaxBytes)
+      throw new ServiceError("Image must be 5 MB or smaller", 413);
+    return output;
+  } catch (error) {
+    if (error instanceof ServiceError) throw error;
+    throw new ServiceError("Choose a valid JPG, PNG or WebP image", 400);
+  }
+}
+
 export async function accountApi(
   request: NextRequest,
   path: string[],
@@ -57,6 +152,52 @@ export async function accountApi(
       });
     return response;
   }
+  if (path[0] === "profile" && path[1] === "avatar" && path.length === 2) {
+    if (request.method !== "POST")
+      return json({ error: "Method not allowed" }, 405);
+    const account = await browserAccount(request, user);
+    await context.limit(`profile:avatar:${account.id}`, 10, 3600);
+    const file = await avatarFile(request);
+    const image = await normalizedAvatar(file);
+    const profileBefore = await accountProfile(account);
+    const avatarPath = `${account.id}/${randomUUID()}.webp`;
+    const storage = admin().storage.from(profileAvatarBucket);
+    const upload = await storage.upload(avatarPath, image, {
+      cacheControl: "31536000",
+      contentType: "image/webp",
+      upsert: false,
+    });
+    if (upload.error)
+      throw new ServiceError(
+        "Profile photo upload failed. Please try again.",
+        503,
+      );
+
+    const profile = await (async () => {
+      try {
+        return required(
+          await admin()
+            .from("profiles")
+            .update({ avatar_path: avatarPath })
+            .eq("id", account.id)
+            .select(
+              "id,display_name,avatar_path,role,name_glow,glow_color,bug_finder,custom_prefix,custom_prefix_icon",
+            )
+            .single(),
+        );
+      } catch (error) {
+        await storage.remove([avatarPath]).catch(() => {});
+        throw error;
+      }
+    })();
+    if (
+      profileBefore.avatar_path &&
+      profileBefore.avatar_path.startsWith(`${account.id}/`) &&
+      profileBefore.avatar_path.split("/").length === 2
+    )
+      await storage.remove([profileBefore.avatar_path]).catch(() => {});
+    return json({ profile });
+  }
   if (
     path[0] === "auth" &&
     path[1] === "initial-password" &&
@@ -92,8 +233,7 @@ export async function accountApi(
     return json({ ok: true });
   }
   if (path[0] === "profile" && path.length === 1) {
-    const account = await user();
-    if (!account) return json({ error: "Log in to manage your account" }, 401);
+    const account = await browserAccount(request, user);
     if (request.method === "GET")
       return json({
         profile: await accountProfile(account),
@@ -102,46 +242,20 @@ export async function accountApi(
     if (request.method === "PATCH") {
       const body = profileUpdateSchema.parse(await context.jsonBody(request));
       const current = await accountProfile(account);
+      if (
+        body.avatarPath !== undefined &&
+        body.avatarPath !== null &&
+        body.avatarPath !== current.avatar_path
+      )
+        return json(
+          { error: "Upload a profile photo through the avatar form" },
+          400,
+        );
       if (body.glowColor !== undefined && !current.name_glow)
         return json(
           { error: "Earn a username glow before choosing its color" },
           403,
         );
-      if (
-        body.avatarPath !== undefined &&
-        body.avatarPath !== null &&
-        body.avatarPath !== current.avatar_path
-      ) {
-        const [ownerId, filename] = body.avatarPath.split("/");
-        if (
-          ownerId !== account.id ||
-          !/^[0-9a-f]{8}-[0-9a-f]{4}-[0-9a-f]{4}-[0-9a-f]{4}-[0-9a-f]{12}\.(jpg|png|webp)$/i.test(
-            filename ?? "",
-          )
-        )
-          return json({ error: "Choose a valid profile photo" }, 400);
-        const uploaded = await admin()
-          .storage.from(profileAvatarBucket)
-          .info(body.avatarPath);
-        if (uploaded.error || !uploaded.data)
-          return json(
-            { error: "Upload your profile photo again" },
-            400,
-          );
-        if (
-          !profileAvatarMimeTypes.includes(
-            uploaded.data.contentType as (typeof profileAvatarMimeTypes)[number],
-          ) ||
-          !uploaded.data.size ||
-          uploaded.data.size > profileAvatarMaxBytes
-        ) {
-          await admin().storage.from(profileAvatarBucket).remove([body.avatarPath]);
-          return json(
-            { error: "Choose an image no larger than 5 MB" },
-            400,
-          );
-        }
-      }
       const profile = required(
         await admin()
           .from("profiles")
@@ -166,7 +280,10 @@ export async function accountApi(
         body.avatarPath !== undefined &&
         body.avatarPath !== current.avatar_path
       ) {
-        if (current.avatar_path?.startsWith(`${account.id}/`))
+        if (
+          current.avatar_path?.startsWith(`${account.id}/`) &&
+          current.avatar_path.split("/").length === 2
+        )
           await admin()
             .storage.from(profileAvatarBucket)
             .remove([current.avatar_path]);
diff --git a/lib/client-api.ts b/lib/client-api.ts
index 93eca17..6e960b8 100644
--- a/lib/client-api.ts
+++ b/lib/client-api.ts
@@ -4,14 +4,23 @@ export async function api<T = Record<string, unknown>>(
   method = body === undefined ? "GET" : "POST",
 ): Promise<T> {
   let response: Response;
+  const formData =
+    typeof FormData !== "undefined" && body instanceof FormData;
   try {
     response = await fetch("/api/v1/" + path, {
       signal: AbortSignal.timeout(30000),
       cache: "no-store",
       method,
       headers:
-        body === undefined ? undefined : { "Content-Type": "application/json" },
-      body: body === undefined ? undefined : JSON.stringify(body),
+        body === undefined || formData
+          ? undefined
+          : { "Content-Type": "application/json" },
+      body:
+        body === undefined
+          ? undefined
+          : typeof FormData !== "undefined" && body instanceof FormData
+            ? body
+            : JSON.stringify(body),
     });
   } catch (error) {
     if (
diff --git a/lib/request-origin.ts b/lib/request-origin.ts
index 10486d4..891290a 100644
--- a/lib/request-origin.ts
+++ b/lib/request-origin.ts
@@ -40,7 +40,14 @@ export function requestOrigin(
   // A different configured host must not redirect a LAN login to localhost.
   if (websiteUrl) {
     const configured = parseOrigin(websiteUrl);
-    if (configured.host === direct.host) return configured.origin;
+    // In production MINEGEO_URL is required and is the trust anchor. Never let
+    // an untrusted Host header choose an OAuth callback or pass the CSRF check.
+    // Development keeps the direct-host fallback for LAN testing.
+    if (
+      configured.host === direct.host ||
+      process.env.NODE_ENV === "production"
+    )
+      return configured.origin;
   }
   return direct.origin;
 }
@@ -63,7 +70,9 @@ export function verifyOrigin(
     if (parsed.pathname !== "/" || parsed.search || parsed.hash) {
       throw new Error("Invalid request origin");
     }
-    const allowed = new Set([requestOrigin(request)]);
+    const allowed = new Set([
+      requestOrigin(request, configuration.websiteUrl),
+    ]);
     for (const value of [
       configuration.websiteUrl,
       ...(configuration.additionalOrigins?.split(",") ?? []),
diff --git a/supabase/migrations/20261015085948_avatar_upload_hardening.sql b/supabase/migrations/20261015085948_avatar_upload_hardening.sql
new file mode 100644
index 0000000..c864e16
--- /dev/null
+++ b/supabase/migrations/20261015085948_avatar_upload_hardening.sql
@@ -0,0 +1,13 @@
+-- The application server is the only writer for public profile avatars. It
+-- validates and re-encodes uploads, applies an account rate limit, and removes
+-- replaced files. Client-side Storage uploads could bypass those controls.
+drop policy if exists "MineGeo users upload their own avatars"
+  on storage.objects;
+drop policy if exists "MineGeo users delete their own avatars"
+  on storage.objects;
+
+update storage.buckets
+set public = true,
+    file_size_limit = 5242880,
+    allowed_mime_types = array['image/webp']
+where id = 'minegeo-avatars';