ABSTRACTThe 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), including two subspecies (E. barbatus nauticus—Pacific and E. barbatus barbatus—Atlantic), is an ice‐obligate Arctic species using sea ice for many 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 (~200 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 hypothesise sea‐ice dynamics and bathymetry had a prominent role in shaping bearded seal genetic structure and diversity. Our analyses of highly differentiated genomic regions can be used to complement the health, physiological, and behavioural 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.