Rapid warming in the Arctic is drastically impacting marine ecosystems, affecting species diversity, distribution, and food web structure. Pelagic Themisto amphipods are a dominant component of the Arctic zooplankton community and represent a key link between secondary producers and marine vertebrates at higher trophic levels. Two co-existing species dominate in the region: Themisto libellula, considered a true Arctic species and Themisto abyssorum, a sub-Arctic, boreal species. Both have exhibited recent changes in abundance and range shifts, likely due to the Atlantification of the Arctic. Many aspects of the ecology and genetic structure of these two species are not well studied, despite their high biomass, importance in the food web and the fact that they are already being affected by rapid climate change in the Arctic. We tested both species for levels of genetic diversity, patterns of spatial genetic structure and demographic history using samples from the Greenland shelf, Fram Strait, and Svalbard. This was achieved using variation at the mitochondrial cytochrome c oxidase subunit 1 gene (mtCOI). These data revealed strikingly different levels of mtCOI diversity: low levels in T. libellula contrasted with high diversity in T. abyssorum. No spatial genetic structure was found, and high levels of connectivity and evidence of historic demographic expansion were exhibited by both species. These patterns of diversity and demographic signatures are likely explained by glaciation events impacting population sizes during the LGM. High population connectivity is likely due to mixing among Themisto populations, caused by the multi-directional currents in the region. The observed low genetic diversity, in combination with its cold adaptions, could cause T. libellula to be more susceptible in the Atlantification of the Arctic. In contrast, high diversity likely increases adaptive potential in T. abyssorum which, combined with its Atlantic affinity, could lead to it benefitting from current warming trends. This study provides new data on the phylogeography of two ecologically important species, which can contribute to predicting how zooplankton communities, species interactions and food web structure will manifest in the Arctic as a result of climate change.