diff --git a/src/core/file_sys/fs.cpp b/src/core/file_sys/fs.cpp
index 769940cf0a..8e0d65a33a 100644
--- a/src/core/file_sys/fs.cpp
+++ b/src/core/file_sys/fs.cpp
@@ -171,4 +171,14 @@ File* HandleTable::GetFile(const std::filesystem::path& host_name) {
     return nullptr;
 }
 
+int HandleTable::GetFileDescriptor(File* file) {
+    std::scoped_lock lock{m_mutex};
+    auto it = std::find(m_files.begin(), m_files.end(), file);
+
+    if (it != m_files.end()) {
+        return std::distance(m_files.begin(), it) + RESERVED_HANDLES;
+    }
+    return 0;
+}
+
 } // namespace Core::FileSys
diff --git a/src/core/file_sys/fs.h b/src/core/file_sys/fs.h
index eeaeaf7810..01003ab8f6 100644
--- a/src/core/file_sys/fs.h
+++ b/src/core/file_sys/fs.h
@@ -9,6 +9,7 @@
 #include <vector>
 #include <tsl/robin_map.h>
 #include "common/io_file.h"
+#include "common/logging/formatter.h"
 
 namespace Core::FileSys {
 
@@ -36,6 +37,14 @@ class MntPoints {
     std::filesystem::path GetHostPath(std::string_view guest_directory,
                                       bool* is_read_only = nullptr);
 
+    const MntPair* GetMountFromHostPath(const std::string& host_path) {
+        std::scoped_lock lock{m_mutex};
+        const auto it = std::ranges::find_if(m_mnt_pairs, [&](const MntPair& mount) {
+            return host_path.starts_with(std::string{fmt::UTF(mount.host_path.u8string()).data});
+        });
+        return it == m_mnt_pairs.end() ? nullptr : &*it;
+    }
+
     const MntPair* GetMount(const std::string& guest_path) {
         std::scoped_lock lock{m_mutex};
         const auto it = std::ranges::find_if(
@@ -75,6 +84,7 @@ class HandleTable {
     void DeleteHandle(int d);
     File* GetFile(int d);
     File* GetFile(const std::filesystem::path& host_name);
+    int GetFileDescriptor(File* file);
 
 private:
     std::vector<File*> m_files;
diff --git a/src/core/libraries/kernel/file_system.cpp b/src/core/libraries/kernel/file_system.cpp
index c4f1e47990..3f99991d55 100644
--- a/src/core/libraries/kernel/file_system.cpp
+++ b/src/core/libraries/kernel/file_system.cpp
@@ -563,12 +563,47 @@ static int GetDents(int fd, char* buf, int nbytes, s64* basep) {
     return sizeof(OrbisKernelDirent);
 }
 
+static int HandleSeparateUpdateDents(int fd, char* buf, int nbytes, s64* basep) {
+    int dir_entries = 0;
+
+    auto* h = Common::Singleton<Core::FileSys::HandleTable>::Instance();
+    auto* mnt = Common::Singleton<Core::FileSys::MntPoints>::Instance();
+    auto* file = h->GetFile(fd);
+    auto update_dir_name = std::string{fmt::UTF(file->m_host_name.u8string()).data};
+    auto mount = mnt->GetMountFromHostPath(update_dir_name);
+    auto suffix = std::string{fmt::UTF(mount->host_path.u8string()).data};
+    auto guest_name = mount->mount + "/" + update_dir_name.substr(suffix.size() + 1);
+
+    size_t pos = update_dir_name.find("-UPDATE");
+    if (pos != std::string::npos) {
+        update_dir_name.erase(pos, 7);
+
+        u32 handle = h->CreateHandle();
+        auto* new_file = h->GetFile(handle);
+        new_file->is_directory = true;
+        new_file->m_guest_name = guest_name;
+        new_file->m_host_name = update_dir_name;
+        if (!std::filesystem::is_directory(new_file->m_host_name)) {
+            h->DeleteHandle(handle);
+            return dir_entries;
+        } else {
+            new_file->dirents = GetDirectoryEntries(new_file->m_host_name);
+            new_file->dirents_index = 0;
+        }
+        new_file->is_opened = true;
+        dir_entries = GetDents(h->GetFileDescriptor(new_file), buf, nbytes, basep);
+        h->DeleteHandle(handle);
+    }
+
+    return dir_entries;
+}
+
 int PS4_SYSV_ABI sceKernelGetdents(int fd, char* buf, int nbytes) {
-    return GetDents(fd, buf, nbytes, nullptr);
+    return GetDents(fd, buf, nbytes, nullptr) + HandleSeparateUpdateDents(fd, buf, nbytes, nullptr);
 }
 
 int PS4_SYSV_ABI sceKernelGetdirentries(int fd, char* buf, int nbytes, s64* basep) {
-    return GetDents(fd, buf, nbytes, basep);
+    return GetDents(fd, buf, nbytes, basep) + HandleSeparateUpdateDents(fd, buf, nbytes, basep);
 }
 
 s64 PS4_SYSV_ABI sceKernelPwrite(int d, void* buf, size_t nbytes, s64 offset) {
diff --git a/src/emulator.cpp b/src/emulator.cpp
index c0b01229a0..0b3f86b01b 100644
--- a/src/emulator.cpp
+++ b/src/emulator.cpp
@@ -105,7 +105,9 @@ void Emulator::Run(const std::filesystem::path& file) {
     // Use the eboot from the separated updates folder if it's there
     std::filesystem::path game_patch_folder = file.parent_path().concat("-UPDATE");
     bool use_game_patch = std::filesystem::exists(game_patch_folder / "sce_sys");
-    std::filesystem::path eboot_path = use_game_patch ? game_patch_folder / file.filename() : file;
+    std::filesystem::path eboot_path = std::filesystem::exists(game_patch_folder / file.filename())
+                                           ? game_patch_folder / file.filename()
+                                           : file;
 
     // Applications expect to be run from /app0 so mount the file's parent path as app0.
     auto* mnt = Common::Singleton<Core::FileSys::MntPoints>::Instance();
diff --git a/src/qt_gui/translations/en.ts b/src/qt_gui/translations/en.ts
index 9bf7c7188a..3c0c7fb068 100644
--- a/src/qt_gui/translations/en.ts
+++ b/src/qt_gui/translations/en.ts
@@ -1159,7 +1159,7 @@
 		<message>
 			<location filename="../settings_dialog.cpp" line="293"/>
 			<source>separateUpdatesCheckBox</source>
-			<translation>Enable Separate Update Folder:\nEnables installing game updates into a separate folder for easy management.</translation>
+			<translation>Enable Separate Update Folder:\nEnables installing game updates into a separate folder for easy management.\nThis can be manually created by adding the extracted update to the game folder with the name "CUSA00000-UPDATE" where the CUSA ID matches the game's ID.</translation>
 		</message>
 		<message>
 			<location filename="../settings_dialog.cpp" line="295"/>