diff --git a/src/core/game_list.cpp b/src/core/game_list.cpp
index 6de20adb4..8a4dbe465 100644
--- a/src/core/game_list.cpp
+++ b/src/core/game_list.cpp
@@ -1201,56 +1201,51 @@ void GameList::CreateDiscSetEntries(const std::vector<std::string>& excluded_pat
 
 std::string GameList::GetCoverImagePathForEntry(const Entry* entry)
 {
-  return GetCoverImagePath(entry->path, entry->serial, entry->GetSaveTitle());
+  return GetCoverImagePath(entry->path, entry->serial, entry->GetSaveTitle(), entry->has_custom_title);
 }
 
-static std::string GetFullCoverPath(std::string_view filename, std::string_view extension)
+static std::string GetFullCoverPath(std::string_view title, std::string_view extension)
 {
-  return fmt::format("{}" FS_OSPATH_SEPARATOR_STR "{}.{}", EmuFolders::Covers, filename, extension);
+  std::string filename = fmt::format("{}.{}", title, extension);
+  Path::SanitizeFileName(&filename);
+  return Path::Combine(EmuFolders::Covers, filename);
 }
 
 std::string GameList::GetCoverImagePath(const std::string_view path, const std::string_view serial,
-                                        const std::string_view title)
+                                        const std::string_view title, bool is_custom_title)
 {
   static constexpr const std::array extensions = {"jpg", "jpeg", "png", "webp"};
   std::string ret;
 
-  for (const char* extension : extensions)
-  {
-    // Prioritize lookup by serial (Most specific)
-    if (!serial.empty())
+  const auto try_name = [&ret](std::string_view name) {
+    for (const char* extension : extensions)
     {
-      std::string cover_path(GetFullCoverPath(serial, extension));
+      std::string cover_path = GetFullCoverPath(name, extension);
       if (FileSystem::FileExists(cover_path.c_str()))
       {
         ret = std::move(cover_path);
-        return ret;
+        return true;
       }
     }
+    return false;
+  };
 
-    // Try file title (for modded games or specific like above)
-    const std::string_view file_title(Path::GetFileTitle(path));
-    if (!file_title.empty() && title != file_title)
-    {
-      std::string cover_path(GetFullCoverPath(file_title, extension));
-      if (FileSystem::FileExists(cover_path.c_str()))
-      {
-        ret = std::move(cover_path);
-        return ret;
-      }
-    }
+  // Check the title first if this is a custom title
+  if (is_custom_title && try_name(title))
+    return ret;
 
-    // Last resort, check the game title
-    if (!title.empty())
-    {
-      std::string cover_path(GetFullCoverPath(title, extension));
-      if (FileSystem::FileExists(cover_path.c_str()))
-      {
-        ret = std::move(cover_path);
-        return ret;
-      }
-    }
-  }
+  // Prioritize lookup by serial (Most specific)
+  if (!serial.empty() && try_name(serial))
+    return ret;
+
+  // Try file title (for modded games or specific like above)
+  const std::string_view file_title = Path::GetFileTitle(path);
+  if (!file_title.empty() && (title != file_title || is_custom_title) && try_name(file_title))
+    return ret;
+
+  // Last resort, check the game title
+  if (!title.empty() && !is_custom_title && try_name(title))
+    return ret;
 
   return ret;
 }
diff --git a/src/core/game_list.h b/src/core/game_list.h
index 0b294af30..34392f94d 100644
--- a/src/core/game_list.h
+++ b/src/core/game_list.h
@@ -143,7 +143,8 @@ std::string FormatTimestamp(std::time_t timestamp);
 TinyString FormatTimespan(std::time_t timespan, bool long_format = false);
 
 std::string GetCoverImagePathForEntry(const Entry* entry);
-std::string GetCoverImagePath(const std::string_view path, const std::string_view serial, const std::string_view title);
+std::string GetCoverImagePath(const std::string_view path, const std::string_view serial, const std::string_view title,
+                              bool is_custom_title);
 std::string GetNewCoverImagePathForEntry(const Entry* entry, const char* new_filename, bool use_serial);
 
 /// Returns a list of (title, entry) for entries matching serials. Titles will match the gamedb title,
diff --git a/src/duckstation-qt/gamelistwidget.cpp b/src/duckstation-qt/gamelistwidget.cpp
index 1e51e1840..b84d3047b 100644
--- a/src/duckstation-qt/gamelistwidget.cpp
+++ b/src/duckstation-qt/gamelistwidget.cpp
@@ -312,9 +312,11 @@ void GameListModel::loadOrGenerateCover(const GameList::Entry* ge)
   QtAsyncTask::create(this, [path = ge->path, serial = ge->serial, save_title = std::string(ge->GetSaveTitle()),
                              display_title = QtUtils::StringViewToQString(ge->GetDisplayTitle(m_show_localized_titles)),
                              placeholder_image = m_placeholder_image, list = this, width = getCoverArtSize(),
-                             height = getCoverArtSize(), scale = m_cover_scale, dpr = m_device_pixel_ratio]() mutable {
+                             height = getCoverArtSize(), scale = m_cover_scale, dpr = m_device_pixel_ratio,
+                             is_custom_title = ge->has_custom_title]() mutable {
     QImage image;
-    loadOrGenerateCover(image, placeholder_image, width, height, scale, dpr, path, serial, save_title, display_title);
+    loadOrGenerateCover(image, placeholder_image, width, height, scale, dpr, path, serial, save_title, display_title,
+                        is_custom_title);
     return [path = std::move(path), image = std::move(image), list, scale]() { list->coverLoaded(path, image, scale); };
   });
 }
@@ -353,9 +355,10 @@ void GameListModel::createPlaceholderImage(QImage& image, const QImage& placehol
 
 void GameListModel::loadOrGenerateCover(QImage& image, const QImage& placeholder_image, int width, int height,
                                         float scale, qreal dpr, const std::string& path, const std::string& serial,
-                                        const std::string& save_title, const QString& display_title)
+                                        const std::string& save_title, const QString& display_title,
+                                        bool is_custom_title)
 {
-  const std::string cover_path(GameList::GetCoverImagePath(path, serial, save_title));
+  const std::string cover_path = GameList::GetCoverImagePath(path, serial, save_title, is_custom_title);
   if (!cover_path.empty())
   {
     image.load(QString::fromStdString(cover_path));
diff --git a/src/duckstation-qt/gamelistwidget.h b/src/duckstation-qt/gamelistwidget.h
index a69ebe94f..6ec97d087 100644
--- a/src/duckstation-qt/gamelistwidget.h
+++ b/src/duckstation-qt/gamelistwidget.h
@@ -130,7 +130,7 @@ private:
 
   static void loadOrGenerateCover(QImage& image, const QImage& placeholder_image, int width, int height, float scale,
                                   qreal dpr, const std::string& path, const std::string& serial,
-                                  const std::string& save_title, const QString& display_title);
+                                  const std::string& save_title, const QString& display_title, bool is_custom_title);
   static void createPlaceholderImage(QImage& image, const QImage& placeholder_image, int width, int height, float scale,
                                      const QString& title);