Wildlife management and conservation requires knowledge about a species’ population structure, diversity, demographic history and adaptive potential. However, often such information is lacking, or based on insufficient and sometimes contrasting data. This is the case for the grey seal (Halichoerus grypus), for which there remain uncertainties regarding subspecies and population delineations, diversity and recent evolutionary history, despite numerous genetic and non-genetic studies. Here, we present the first range- and genome-wide population genomic analysis of grey seals based on 3,812 nuclear SNP markers genotyped in 188 samples from 17 distinct localities. Our analyses support the existence of three main grey seal populations centred in the NW Atlantic, NE Atlantic and Baltic Sea, but also point to the existence of previously unrecognised substructure within the NE Atlantic, in particular separating grey seals sampled in Iceland, Norway and Russia from the core NE Atlantic population inhabiting the wider North Sea region. We detected remarkably low levels of genetic diversity in NW Atlantic grey seals, which may be the result of evolutionary founder effects, as well as more recent historic hunting and culling. We also found some localities that deviate from the general isolation by distance pattern, likely reflecting wide-scale metapopulation dynamics associated with recolonisation and recovery of grey seals in regions where they were historically extirpated. Our genetic results allow us to identify at least six grey seal management units across the species’ Atlantic range, but also highlights knowledge gaps that should be addressed in future research into this species.