In the aftermath of the Euro-crisis, refugee crisis and Brexit, Europe’s finalité politique once again became a topic of heated debate. Both Eurosceptic nationalists and defenders of the EU appeal to the democratic principle of popular sovereignty, but they offer conflicting interpretations. This study seeks to offer a fine-grained framework to analyze this normative conflict of sovereignty. I distinguish four conceptions of popular sovereignty in Europe’s transnational polity; each is linked to a parliamentary arrangement. First, national popular sovereignty proposes a safeguarding of sovereign nation-states. Second, European popular sovereignty suggests that decision-making power should shift from the member-states to a European superstate. Third, simultaneous popular sovereignty suggests that national peoples and EU citizens should be represented in the EU. Fourth, shared popular sovereignty points toward national parliamentarians being the central locus of democratic authority in the EU. These conceptions thus result in conflicting institutional prescriptions.