The article draws comparisons between inter-parliamentary cooperation in the European Union and at the international level. It recognises that, notwithstanding a strong international imprint, inter-parliamentary relations in the EU have gradually experienced somewhat distinctive pushes, deeply embedded in the unique constitutional arrangement of the Union. On the one hand, the composite nature of EU constitutionalism, and its impact on parliaments’ relationship with the democratic oversight rationale, have exercised a major influence on the aims and scope of inter-parliamentary cooperation. On the other hand, from the organisational point of view, the distinctive structure of parliamentary representation in the EU has pushed inter-parliamentary arrangements into a multi-layered design, consisting of a large variety of vertical formats. The article argues that inter-parliamentary cooperation in the EU is expected to act as a sui generis practice when compared to apparently similar forms of transnational dialogue amongst parliaments. In theory, at least, the EU sets ideal conditions for fulfilling an authentic collective parliamentary dimension, instrumental to the democratic oversight of the executives. Instead, focusing on the practice, the full potential of EU inter-parliamentarism is not yet fulfilled, for two set of reasons: the unresolved ambiguities over its contribution to parliamentary democracy and the lack of a real capacity to depart from the formats of international parliamentary institutions.