Rapid warming in the Arctic is drastically impacting marine ecosystems, affecting species diversity, distribution, and food web structure. Pelagic Themisto amphipods are dominant in the Arctic zooplankton community and represent a key link between secondary producers and 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. 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. We tested both species for levels of genetic diversity, patterns of spatial genetic structure and demographic history in the Greenland shelf, Fram Strait, and Svalbard. This was achieved using variation on 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 higher 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. The diversity and demographic signatures are likely explained by glaciation events impacting population sizes during the last glacial maximum. High population connectivity is likely due to current-induced mixing among Themisto populations. The observed low genetic diversity, in combination with its cold adaptions, could cause T. libellula to be more susceptible to 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 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.