Understanding how populations diverge is one of the oldest and most compelling questions in evolutionary biology. An in depth understanding of how this process operates in planktonic marine animals, where barriers for gene flow are seemingly absent, is critical to understanding the past, present, and future of ocean life. Mnemiopsis plays an important ecological role in its native habitat along the Atlantic coast of the Americas and is highly destructive in its non-native habitats in European waters. Although historical literature described three species of Mnemiopsis, the lack of stable morphological characters has led to the collapse of this group into a single species, Mnemiopsis leidyi. We generate high-quality reference genomes and use a whole-genome sequencing approach to reveal that there are two species of Mnemiopsis along its native range and show that historical divergence between the two species coincides with historical glacial melting. We define a hybridization zone between species and highlight that environmental sensing genes likely contribute to the invasive success of Mnemiopsis. Overall, this study provides insights into the fundamental question of how holopelagic species arise without clear barriers to gene flow and sheds light on the genomic mechanisms important for invasion success in a highly invasive species.