diff --git a/src/gui/Application.cpp b/src/gui/Application.cpp
index 402b50c3d..969f623d7 100644
--- a/src/gui/Application.cpp
+++ b/src/gui/Application.cpp
@@ -51,6 +51,7 @@ enum Application::SocketCmd : quint32
 {
     OpenFiles = 1,
     LockAll,
+    Unlock,
 };
 
 Application::Application(int& argc, char** argv)
@@ -327,8 +328,7 @@ void Application::socketReadyRead()
     }
 
     SocketCmd id;
-    // manual reinterpret_cast not needed for Qt 5.14+
-    in >> reinterpret_cast<typename std::underlying_type<SocketCmd>::type&>(id);
+    in >> id;
 
     switch (id) {
     case SocketCmd::OpenFiles: {
@@ -345,6 +345,11 @@ void Application::socketReadyRead()
     case SocketCmd::LockAll:
         getMainWindow()->lockAllDatabases();
         break;
+    case SocketCmd::Unlock:
+        QString filename, password, keyfile;
+        in >> filename >> password >> keyfile;
+        emit openFile(filename, password, keyfile);
+        break;
     }
 
     socket->deleteLater();
@@ -352,10 +357,6 @@ void Application::socketReadyRead()
 
 bool Application::isAlreadyRunning() const
 {
-#ifdef QT_DEBUG
-    // In DEBUG mode we can run unlimited instances
-    return false;
-#endif
     return config()->get(Config::SingleInstance).toBool() && m_alreadyRunning;
 }
 
@@ -392,7 +393,7 @@ bool Application::sendSocketCommand(SocketCmd id, const std::function<void(QData
  */
 bool Application::sendFileNamesToRunningInstance(const QStringList& fileNames)
 {
-    return this->sendSocketCommand(SocketCmd::OpenFiles, [fileNames](QDataStream& out) { out << fileNames; });
+    return this->sendSocketCommand(SocketCmd::OpenFiles, [&](QDataStream& out) { out << fileNames; });
 }
 
 /**
@@ -405,6 +406,17 @@ bool Application::sendLockToInstance()
     return this->sendSocketCommand(SocketCmd::LockAll, [](QDataStream&) { /* No Data */ });
 }
 
+/**
+ * Open and unlock a database file in the running instance
+ *
+ * @return true if the instance receives the request
+ */
+bool Application::sendUnlockToInstance(const QString& filename, const QString& password, const QString& keyfile)
+{
+    return this->sendSocketCommand(SocketCmd::Unlock,
+                                   [&](QDataStream& out) { out << filename << password << keyfile; });
+}
+
 bool Application::isDarkTheme() const
 {
     return m_darkTheme;
diff --git a/src/gui/Application.h b/src/gui/Application.h
index 4d7a87fca..b00f8ce99 100644
--- a/src/gui/Application.h
+++ b/src/gui/Application.h
@@ -53,11 +53,12 @@ public:
 
     bool sendFileNamesToRunningInstance(const QStringList& fileNames);
     bool sendLockToInstance();
+    bool sendUnlockToInstance(const QString& filename, const QString& password = {}, const QString& keyfile = {});
 
     void restart();
 
 signals:
-    void openFile(const QString& filename);
+    void openFile(const QString& filename, const QString& password = {}, const QString& keyfile = {});
     void anotherInstanceStarted();
     void applicationActivated();
     void quitSignalReceived();
diff --git a/src/gui/MainWindow.cpp b/src/gui/MainWindow.cpp
index a051187d6..067f7250c 100644
--- a/src/gui/MainWindow.cpp
+++ b/src/gui/MainWindow.cpp
@@ -661,8 +661,8 @@ MainWindow::MainWindow()
 
     connect(qApp, SIGNAL(anotherInstanceStarted()), this, SLOT(bringToFront()));
     connect(qApp, SIGNAL(applicationActivated()), this, SLOT(bringToFront()));
-    connect(qApp, SIGNAL(openFile(QString)), this, SLOT(openDatabase(QString)));
     connect(qApp, SIGNAL(quitSignalReceived()), this, SLOT(appExit()), Qt::DirectConnection);
+    connect(static_cast<Application*>(qApp), &Application::openFile, this, &MainWindow::openDatabase);
 
     // Setup the status bar
     statusBar()->setFixedHeight(24);
diff --git a/src/main.cpp b/src/main.cpp
index 2c4da4c1f..f9af22ecc 100644
--- a/src/main.cpp
+++ b/src/main.cpp
@@ -49,6 +49,18 @@ Q_IMPORT_PLUGIN(QXcbIntegrationPlugin)
 #include <windows.h>
 #endif
 
+namespace
+{
+    QString promptPassword()
+    {
+        // we always need consume a line of STDIN if --pw-stdin is set to clear out the
+        // buffer for native messaging, even if the specified file does not exist
+        QTextStream out(stdout, QIODevice::WriteOnly);
+        out << QObject::tr("Database password: ") << Qt::flush;
+        return Utils::getPassword();
+    }
+} // namespace
+
 int main(int argc, char** argv)
 {
     QT_REQUIRE_VERSION(argc, argv, QT_VERSION_STR)
@@ -140,9 +152,14 @@ int main(int argc, char** argv)
         }
     }
 #endif
+    Utils::setDefaultTextStreams();
+
+    const bool pwstdin = parser.isSet(pwstdinOption);
+    const QString keyfile = parser.value(keyfileOption);
 
     // Process single instance and early exit if already running
     if (app.isAlreadyRunning()) {
+        qWarning() << QObject::tr("Another instance of KeePassXC is already running.").toUtf8().constData();
         if (parser.isSet(lockOption)) {
             if (app.sendLockToInstance()) {
                 qInfo() << QObject::tr("Databases have been locked.").toUtf8().constData();
@@ -151,11 +168,13 @@ int main(int argc, char** argv)
                 return EXIT_FAILURE;
             }
         } else {
-            if (!fileNames.isEmpty()) {
-                app.sendFileNamesToRunningInstance(fileNames);
+            for (const QString& filename : fileNames) {
+                QString password;
+                if (pwstdin) {
+                    password = promptPassword();
+                }
+                app.sendUnlockToInstance(filename, password, keyfile);
             }
-
-            qWarning() << QObject::tr("Another instance of KeePassXC is already running.").toUtf8().constData();
         }
         return EXIT_SUCCESS;
     }
@@ -176,8 +195,6 @@ int main(int argc, char** argv)
         return EXIT_FAILURE;
     }
 
-    Utils::setDefaultTextStreams();
-
     // Apply the configured theme before creating any GUI elements
     app.applyTheme();
 
@@ -195,17 +212,12 @@ int main(int argc, char** argv)
     // This ensures any top-level windows (Main Window, Modal Dialogs, etc.) are excluded from screenshots
     mainWindow.setAllowScreenCapture(parser.isSet(allowScreenCaptureOption));
 
-    const bool pwstdin = parser.isSet(pwstdinOption);
     for (const QString& filename : fileNames) {
         QString password;
         if (pwstdin) {
-            // we always need consume a line of STDIN if --pw-stdin is set to clear out the
-            // buffer for native messaging, even if the specified file does not exist
-            QTextStream out(stdout, QIODevice::WriteOnly);
-            out << QObject::tr("Database password: ") << Qt::flush;
-            password = Utils::getPassword();
+            password = promptPassword();
         }
-        mainWindow.openDatabase(filename, password, parser.value(keyfileOption));
+        mainWindow.openDatabase(filename, password, keyfile);
     }
 
     // start minimized if configured