diff --git a/Userland/DevTools/HackStudio/LanguageClient.cpp b/Userland/DevTools/HackStudio/LanguageClient.cpp
index 54c4f9593ad..58af26c956d 100644
--- a/Userland/DevTools/HackStudio/LanguageClient.cpp
+++ b/Userland/DevTools/HackStudio/LanguageClient.cpp
@@ -64,7 +64,7 @@ void LanguageClient::open_file(ByteString const& path, int fd)
 {
     if (!m_connection_wrapper.connection())
         return;
-    m_connection_wrapper.connection()->async_file_opened(path, fd);
+    m_connection_wrapper.connection()->async_file_opened(path, MUST(IPC::File::clone_fd(fd)));
 }
 
 void LanguageClient::set_file_content(ByteString const& path, ByteString const& content)
diff --git a/Userland/Libraries/LibGUI/Window.cpp b/Userland/Libraries/LibGUI/Window.cpp
index f274f4774de..d79b239c265 100644
--- a/Userland/Libraries/LibGUI/Window.cpp
+++ b/Userland/Libraries/LibGUI/Window.cpp
@@ -983,7 +983,7 @@ void Window::set_current_backing_store(WindowBackingStore& backing_store, bool f
         m_window_id,
         32,
         bitmap.pitch(),
-        bitmap.anonymous_buffer().fd(),
+        MUST(IPC::File::clone_fd(bitmap.anonymous_buffer().fd())),
         backing_store.serial(),
         bitmap.has_alpha_channel(),
         bitmap.size(),
diff --git a/Userland/Libraries/LibGfx/ShareableBitmap.cpp b/Userland/Libraries/LibGfx/ShareableBitmap.cpp
index 26f87a2195b..c8e4df017f4 100644
--- a/Userland/Libraries/LibGfx/ShareableBitmap.cpp
+++ b/Userland/Libraries/LibGfx/ShareableBitmap.cpp
@@ -30,7 +30,7 @@ ErrorOr<void> encode(Encoder& encoder, Gfx::ShareableBitmap const& shareable_bit
         return {};
 
     auto& bitmap = *shareable_bitmap.bitmap();
-    TRY(encoder.encode(IPC::File(bitmap.anonymous_buffer().fd())));
+    TRY(encoder.encode(TRY(IPC::File::clone_fd(bitmap.anonymous_buffer().fd()))));
     TRY(encoder.encode(bitmap.size()));
     TRY(encoder.encode(static_cast<u32>(bitmap.scale())));
     TRY(encoder.encode(static_cast<u32>(bitmap.format())));
diff --git a/Userland/Libraries/LibIPC/Decoder.cpp b/Userland/Libraries/LibIPC/Decoder.cpp
index 3e2ac066776..1abd370ce5c 100644
--- a/Userland/Libraries/LibIPC/Decoder.cpp
+++ b/Userland/Libraries/LibIPC/Decoder.cpp
@@ -91,7 +91,7 @@ template<>
 ErrorOr<File> decode(Decoder& decoder)
 {
     int fd = TRY(decoder.socket().receive_fd(O_CLOEXEC));
-    return File { fd, File::ConstructWithReceivedFileDescriptor };
+    return File::adopt_fd(fd);
 }
 
 template<>
diff --git a/Userland/Libraries/LibIPC/Encoder.cpp b/Userland/Libraries/LibIPC/Encoder.cpp
index 0469eba2e14..51ac2efbeb2 100644
--- a/Userland/Libraries/LibIPC/Encoder.cpp
+++ b/Userland/Libraries/LibIPC/Encoder.cpp
@@ -105,10 +105,7 @@ ErrorOr<void> encode(Encoder& encoder, URL::URL const& value)
 template<>
 ErrorOr<void> encode(Encoder& encoder, File const& file)
 {
-    int fd = file.fd();
-
-    if (fd != -1)
-        fd = TRY(Core::System::dup(fd));
+    int fd = file.take_fd();
 
     TRY(encoder.append_file_descriptor(fd));
     return {};
@@ -127,7 +124,7 @@ ErrorOr<void> encode(Encoder& encoder, Core::AnonymousBuffer const& buffer)
 
     if (buffer.is_valid()) {
         TRY(encoder.encode_size(buffer.size()));
-        TRY(encoder.encode(IPC::File { buffer.fd() }));
+        TRY(encoder.encode(TRY(IPC::File::clone_fd(buffer.fd()))));
     }
 
     return {};
diff --git a/Userland/Libraries/LibIPC/Encoder.h b/Userland/Libraries/LibIPC/Encoder.h
index d3364f9cfbc..6813c8af3fc 100644
--- a/Userland/Libraries/LibIPC/Encoder.h
+++ b/Userland/Libraries/LibIPC/Encoder.h
@@ -13,6 +13,7 @@
 #include <AK/Variant.h>
 #include <LibCore/SharedCircularQueue.h>
 #include <LibIPC/Concepts.h>
+#include <LibIPC/File.h>
 #include <LibIPC/Forward.h>
 #include <LibIPC/Message.h>
 #include <LibURL/Forward.h>
@@ -148,7 +149,8 @@ ErrorOr<void> encode(Encoder& encoder, T const& hashmap)
 template<Concepts::SharedSingleProducerCircularQueue T>
 ErrorOr<void> encode(Encoder& encoder, T const& queue)
 {
-    return encoder.encode(IPC::File { queue.fd() });
+    TRY(encoder.encode(TRY(IPC::File::clone_fd(queue.fd()))));
+    return {};
 }
 
 template<Concepts::Optional T>
diff --git a/Userland/Libraries/LibIPC/File.h b/Userland/Libraries/LibIPC/File.h
index 15f70a69d8e..ab565e7a400 100644
--- a/Userland/Libraries/LibIPC/File.h
+++ b/Userland/Libraries/LibIPC/File.h
@@ -10,7 +10,7 @@
 #include <AK/Noncopyable.h>
 #include <AK/StdLibExtras.h>
 #include <LibCore/File.h>
-#include <unistd.h>
+#include <LibCore/System.h>
 
 namespace IPC {
 
@@ -18,36 +18,26 @@ class File {
     AK_MAKE_NONCOPYABLE(File);
 
 public:
-    // Must have a default constructor, because LibIPC
-    // default-constructs arguments prior to decoding them.
     File() = default;
 
-    // Intentionally not `explicit`.
-    File(int fd)
-        : m_fd(fd)
+    static File adopt_file(NonnullOwnPtr<Core::File> file)
     {
+        return File(file->leak_fd(Badge<File> {}));
     }
 
-    // Tagged constructor for fd's that should be closed on destruction unless take_fd() is called.
-    // Note that the tags are the same, this is intentional to allow expressive invocation.
-    enum Tag {
-        ConstructWithReceivedFileDescriptor = 1,
-        CloseAfterSending = 1,
-    };
-    File(int fd, Tag)
-        : m_fd(fd)
-        , m_close_on_destruction(true)
+    static File adopt_fd(int fd)
     {
+        return File(fd);
     }
 
-    explicit File(Core::File& file)
-        : File(file.leak_fd(Badge<File> {}), CloseAfterSending)
+    static ErrorOr<File> clone_fd(int fd)
     {
+        int new_fd = TRY(Core::System::dup(fd));
+        return File(new_fd);
     }
 
     File(File&& other)
         : m_fd(exchange(other.m_fd, -1))
-        , m_close_on_destruction(exchange(other.m_close_on_destruction, false))
     {
     }
 
@@ -55,15 +45,14 @@ public:
     {
         if (this != &other) {
             m_fd = exchange(other.m_fd, -1);
-            m_close_on_destruction = exchange(other.m_close_on_destruction, false);
         }
         return *this;
     }
 
     ~File()
     {
-        if (m_close_on_destruction && m_fd != -1)
-            close(m_fd);
+        if (m_fd != -1)
+            (void)Core::System::close(m_fd);
     }
 
     int fd() const { return m_fd; }
@@ -75,8 +64,12 @@ public:
     }
 
 private:
+    explicit File(int fd)
+        : m_fd(fd)
+    {
+    }
+
     mutable int m_fd { -1 };
-    bool m_close_on_destruction { false };
 };
 
 }
diff --git a/Userland/Libraries/LibWeb/HTML/MessagePort.cpp b/Userland/Libraries/LibWeb/HTML/MessagePort.cpp
index 9c95839ce0b..6cf22e73735 100644
--- a/Userland/Libraries/LibWeb/HTML/MessagePort.cpp
+++ b/Userland/Libraries/LibWeb/HTML/MessagePort.cpp
@@ -80,12 +80,12 @@ WebIDL::ExceptionOr<void> MessagePort::transfer_steps(HTML::TransferDataHolder&
         // 2. Set dataHolder.[[RemotePort]] to remotePort.
         auto fd = MUST(m_socket->release_fd());
         m_socket = nullptr;
-        data_holder.fds.append(IPC::File(fd, IPC::File::CloseAfterSending));
+        data_holder.fds.append(IPC::File::adopt_fd(fd));
         data_holder.data.append(IPC_FILE_TAG);
 
         auto fd_passing_socket = MUST(m_fd_passing_socket->release_fd());
         m_fd_passing_socket = nullptr;
-        data_holder.fds.append(IPC::File(fd_passing_socket, IPC::File::CloseAfterSending));
+        data_holder.fds.append(IPC::File::adopt_fd(fd_passing_socket));
         data_holder.data.append(IPC_FILE_TAG);
     }
 
diff --git a/Userland/Libraries/LibWeb/HTML/SelectedFile.cpp b/Userland/Libraries/LibWeb/HTML/SelectedFile.cpp
index be31a4e1b32..5b059398a90 100644
--- a/Userland/Libraries/LibWeb/HTML/SelectedFile.cpp
+++ b/Userland/Libraries/LibWeb/HTML/SelectedFile.cpp
@@ -20,7 +20,7 @@ ErrorOr<SelectedFile> SelectedFile::from_file_path(ByteString const& file_path)
     auto name = LexicalPath::basename(file_path);
 
     auto file = TRY(Core::File::open(file_path, Core::File::OpenMode::Read));
-    return SelectedFile { move(name), IPC::File { *file } };
+    return SelectedFile { move(name), IPC::File::adopt_file(move(file)) };
 }
 
 SelectedFile::SelectedFile(ByteString name, ByteBuffer contents)
diff --git a/Userland/Libraries/LibWeb/Page/Page.h b/Userland/Libraries/LibWeb/Page/Page.h
index 7f60ab4ad24..8df6cdd40a8 100644
--- a/Userland/Libraries/LibWeb/Page/Page.h
+++ b/Userland/Libraries/LibWeb/Page/Page.h
@@ -315,7 +315,7 @@ public:
 
     virtual void page_did_change_audio_play_state(HTML::AudioPlayState) { }
 
-    virtual WebView::SocketPair request_worker_agent() { return { -1, -1 }; }
+    virtual WebView::SocketPair request_worker_agent() { return { IPC::File {}, IPC::File {} }; }
 
     virtual void inspector_did_load() { }
     virtual void inspector_did_select_dom_node([[maybe_unused]] i32 node_id, [[maybe_unused]] Optional<CSS::Selector::PseudoElement::Type> const& pseudo_element) { }
diff --git a/Userland/Libraries/LibWeb/Worker/WebWorkerClient.cpp b/Userland/Libraries/LibWeb/Worker/WebWorkerClient.cpp
index 418f97fd57e..943b23c140b 100644
--- a/Userland/Libraries/LibWeb/Worker/WebWorkerClient.cpp
+++ b/Userland/Libraries/LibWeb/Worker/WebWorkerClient.cpp
@@ -22,8 +22,8 @@ WebWorkerClient::WebWorkerClient(NonnullOwnPtr<Core::LocalSocket> socket)
 WebView::SocketPair WebWorkerClient::dup_sockets()
 {
     WebView::SocketPair pair;
-    pair.socket = IPC::File(MUST(Core::System::dup(socket().fd().value())), IPC::File::CloseAfterSending);
-    pair.fd_passing_socket = IPC::File(MUST(Core::System::dup(fd_passing_socket().fd().value())), IPC::File::CloseAfterSending);
+    pair.socket = MUST(IPC::File::clone_fd(socket().fd().value()));
+    pair.fd_passing_socket = MUST(IPC::File::clone_fd(fd_passing_socket().fd().value()));
     return pair;
 }
 
diff --git a/Userland/Libraries/LibWebView/OutOfProcessWebView.cpp b/Userland/Libraries/LibWebView/OutOfProcessWebView.cpp
index 981666f75f7..a2c1ab518c2 100644
--- a/Userland/Libraries/LibWebView/OutOfProcessWebView.cpp
+++ b/Userland/Libraries/LibWebView/OutOfProcessWebView.cpp
@@ -44,7 +44,7 @@ OutOfProcessWebView::OutOfProcessWebView()
         if (file.is_error())
             client().async_handle_file_return(m_client_state.page_index, file.error().code(), {}, request_id);
         else
-            client().async_handle_file_return(m_client_state.page_index, 0, IPC::File(file.value().stream()), request_id);
+            client().async_handle_file_return(m_client_state.page_index, 0, IPC::File::adopt_file(file.release_value().release_stream()), request_id);
     };
 
     on_scroll_by_delta = [this](auto x_delta, auto y_delta) {
diff --git a/Userland/Libraries/LibWebView/ViewImplementation.cpp b/Userland/Libraries/LibWebView/ViewImplementation.cpp
index c70a91bc106..bba1b31e6ae 100644
--- a/Userland/Libraries/LibWebView/ViewImplementation.cpp
+++ b/Userland/Libraries/LibWebView/ViewImplementation.cpp
@@ -32,7 +32,7 @@ ViewImplementation::ViewImplementation()
         if (file.is_error())
             client().async_handle_file_return(page_id(), file.error().code(), {}, request_id);
         else
-            client().async_handle_file_return(page_id(), 0, IPC::File(*file.value()), request_id);
+            client().async_handle_file_return(page_id(), 0, IPC::File::adopt_file(file.release_value()), request_id);
     };
 }
 
diff --git a/Userland/Libraries/LibWebView/WebContentClient.cpp b/Userland/Libraries/LibWebView/WebContentClient.cpp
index 3601d931dc0..609eb9d2c2c 100644
--- a/Userland/Libraries/LibWebView/WebContentClient.cpp
+++ b/Userland/Libraries/LibWebView/WebContentClient.cpp
@@ -665,7 +665,7 @@ Messages::WebContentClient::RequestWorkerAgentResponse WebContentClient::request
             return view->on_request_worker_agent();
     }
 
-    return WebView::SocketPair { -1, -1 };
+    return WebView::SocketPair { IPC::File {}, IPC::File {} };
 }
 
 Optional<ViewImplementation&> WebContentClient::view_for_page_id(u64 page_id, SourceLocation location)
diff --git a/Userland/Services/FileSystemAccessServer/ConnectionFromClient.cpp b/Userland/Services/FileSystemAccessServer/ConnectionFromClient.cpp
index a22d413007f..f8852f1beb4 100644
--- a/Userland/Services/FileSystemAccessServer/ConnectionFromClient.cpp
+++ b/Userland/Services/FileSystemAccessServer/ConnectionFromClient.cpp
@@ -81,7 +81,7 @@ void ConnectionFromClient::request_file_handler(i32 request_id, i32 window_serve
             dbgln("FileSystemAccessServer: Couldn't open {}, error {}", path, file.error());
             async_handle_prompt_end(request_id, file.error().code(), Optional<IPC::File> {}, path);
         } else {
-            async_handle_prompt_end(request_id, 0, IPC::File(*file.release_value()), path);
+            async_handle_prompt_end(request_id, 0, IPC::File::adopt_file(file.release_value()), path);
         }
     } else {
         async_handle_prompt_end(request_id, EPERM, Optional<IPC::File> {}, path);
@@ -138,7 +138,7 @@ void ConnectionFromClient::prompt_helper(i32 request_id, Optional<ByteString> co
 
             m_approved_files.set(user_picked_file.value(), new_permissions);
 
-            async_handle_prompt_end(request_id, 0, IPC::File(*file.release_value()), user_picked_file);
+            async_handle_prompt_end(request_id, 0, IPC::File::adopt_file(file.release_value()), user_picked_file);
         }
     } else {
         async_handle_prompt_end(request_id, ECANCELED, Optional<IPC::File> {}, Optional<ByteString> {});
diff --git a/Userland/Services/RequestServer/ConnectionFromClient.cpp b/Userland/Services/RequestServer/ConnectionFromClient.cpp
index 4ee6e093fc9..ca01cd995bb 100644
--- a/Userland/Services/RequestServer/ConnectionFromClient.cpp
+++ b/Userland/Services/RequestServer/ConnectionFromClient.cpp
@@ -42,10 +42,12 @@ void ConnectionFromClient::die()
 
 Messages::RequestServer::ConnectNewClientResponse ConnectionFromClient::connect_new_client()
 {
+    Messages::RequestServer::ConnectNewClientResponse error_response = { IPC::File {}, IPC::File {} };
+
     int socket_fds[2] {};
     if (auto err = Core::System::socketpair(AF_LOCAL, SOCK_STREAM, 0, socket_fds); err.is_error()) {
         dbgln("Failed to create client socketpair: {}", err.error());
-        return { -1, -1 };
+        return error_response;
     }
 
     auto client_socket_or_error = Core::LocalSocket::adopt_fd(socket_fds[0]);
@@ -53,7 +55,7 @@ Messages::RequestServer::ConnectNewClientResponse ConnectionFromClient::connect_
         close(socket_fds[0]);
         close(socket_fds[1]);
         dbgln("Failed to adopt client socket: {}", client_socket_or_error.error());
-        return { -1, -1 };
+        return error_response;
     }
     auto client_socket = client_socket_or_error.release_value();
     // Note: A ref is stored in the static s_connections map
@@ -63,7 +65,7 @@ Messages::RequestServer::ConnectNewClientResponse ConnectionFromClient::connect_
     if (auto err = Core::System::socketpair(AF_LOCAL, SOCK_STREAM, 0, fd_passing_socket_fds); err.is_error()) {
         close(socket_fds[1]);
         dbgln("Failed to create fd-passing socketpair: {}", err.error());
-        return { -1, -1 };
+        return error_response;
     }
 
     auto fd_passing_socket_or_error = Core::LocalSocket::adopt_fd(fd_passing_socket_fds[0]);
@@ -73,12 +75,12 @@ Messages::RequestServer::ConnectNewClientResponse ConnectionFromClient::connect_
         close(fd_passing_socket_fds[0]);
         close(fd_passing_socket_fds[1]);
         dbgln("Failed to adopt fd-passing socket: {}", fd_passing_socket_or_error.error());
-        return { -1, -1 };
+        return error_response;
     }
     auto fd_passing_socket = fd_passing_socket_or_error.release_value();
     client->set_fd_passing_socket(move(fd_passing_socket));
 
-    return { IPC::File(socket_fds[1], IPC::File::CloseAfterSending), IPC::File(fd_passing_socket_fds[1], IPC::File::CloseAfterSending) };
+    return { IPC::File::adopt_fd(socket_fds[1]), IPC::File::adopt_fd(fd_passing_socket_fds[1]) };
 }
 
 Messages::RequestServer::IsSupportedProtocolResponse ConnectionFromClient::is_supported_protocol(ByteString const& protocol)
@@ -110,7 +112,7 @@ void ConnectionFromClient::start_request(i32 request_id, ByteString const& metho
     auto id = request->id();
     auto fd = request->request_fd();
     m_requests.set(id, move(request));
-    (void)post_message(Messages::RequestClient::RequestStarted(request_id, IPC::File(fd, IPC::File::CloseAfterSending)));
+    (void)post_message(Messages::RequestClient::RequestStarted(request_id, IPC::File::adopt_fd(fd)));
 }
 
 Messages::RequestServer::StopRequestResponse ConnectionFromClient::stop_request(i32 request_id)
diff --git a/Userland/Services/WebWorker/ConnectionFromClient.cpp b/Userland/Services/WebWorker/ConnectionFromClient.cpp
index 4110e4a557a..11e39a42bb4 100644
--- a/Userland/Services/WebWorker/ConnectionFromClient.cpp
+++ b/Userland/Services/WebWorker/ConnectionFromClient.cpp
@@ -31,7 +31,7 @@ void ConnectionFromClient::request_file(Web::FileRequest request)
     if (file.is_error())
         handle_file_return(file.error().code(), {}, request_id);
     else
-        handle_file_return(0, IPC::File(*file.value()), request_id);
+        handle_file_return(0, IPC::File::adopt_file(file.release_value()), request_id);
 }
 
 ConnectionFromClient::ConnectionFromClient(NonnullOwnPtr<Core::LocalSocket> socket)