Assessing genetic structure and diversity in wildlife is particularly important in the context of climate change. The Arctic is rapidly warming, and endemic species must adapt quickly or face significant threats to persistence. Bowhead whales (Balaena mysticetus) and narwhals (Monodon monoceros) are two long-lived Arctic species with similar habitat requirements and are often seen together in the Canadian Arctic. Although their ranges overlap extensively, bowhead whales experienced significantly greater commercial whaling mortality than narwhals over several centuries. The similar habitat requirements but different harvest histories of these two species provide an opportunity to examine present-day genetic diversity and the demographic and genetic consequences of commercial whaling. We whole-genome resequenced contemporary Canadian Arctic bowhead whales and narwhals to delineate population structure and reconstruct demographic history. We found higher genetic diversity in bowhead whales compared to narwhals. However, bowhead whale effective population size sharply declined contemporaneously with the intense commercial whaling period. Narwhals, in contrast, exhibited recent growth in effective population size, likely reflecting exposure to limited opportunistic commercial harvest. Bowhead whales will likely continue to experience significant genetic drift in the future, leading to the erosion of genetic diversity. In contrast, narwhals do not seem to be at imminent risk of losing their current levels of genetic variation due to their long-term low effective population size and lack of evidence for a recent decline. This work highlights the importance of considering population trajectories in addition to genetic diversity when assessing the genetics of populations for conservation and management purposes.