The Arctic environment plays a critical role in the global climate system and marine biodiversity. The region’s ice-covered expanses provide essential breeding and feeding grounds for a diverse assemblage of marine species, who have adapted to thrive in these harsh conditions and consequently are under threat from global warming. The bearded seal (Erignathus barbatus) is an ice-obligate Arctic species using sea-ice for all aspects of its life-history, rendering it particularly vulnerable to sea-ice loss. It is one of the least studied and hence enigmatic of the Arctic marine mammals, with little knowledge regarding genetic structure, diversity, adaptations and demographic history, consequently hampering management and conservation efforts. Here, we sequenced 70 whole nuclear genomes from across most of the species’ circumpolar range, finding significant genetic structure between the Pacific and the Atlantic subspecies, which diverged during the Penultimate Glacial Period (~192 KYA). Remarkably, we found fine-scale genetic structure within both subspecies, with at least two distinct populations in the Pacific and three in the Atlantic. We hypothesize sea-ice dynamics and bathymetry had a prominent role of in shaping bearded seal genetic structure and diversity. Resulting genomic data can be used to complement the health, physiological, and behavioral research needed to conserve this species. In addition, we provide recommendations for management units that can be used to more specifically assess climatic and anthropogenic impacts on bearded seal populations.