Information about the distribution of genomic variation within and between nesting locations of waterfowl can aid in defining populations and conservation plans and inform harvest management. Identification of locations where shifts in allelic diversity occur is particularly important for Arctic nesting species nesting, a region currently experiencing rapid change associated with climate and other factors. Here, we build upon previous investigations on spatial patterns of genetic variation in a largely migratory, circumpolar breeding sea duck, the common eider (Somateria mollissima) through inclusion of additional sample locations and genomic markers. We analyzed double-digest restriction site-associated DNA sequences from 309 common eiders to estimate genetic variation within, and differentiation among, 21 nesting locations across North America. Our results corroborate previous evidence of four genetic groups that coincide with colonies that share similar winter areas. We found deeper genomic differences between common eiders wintering in the west (Pacific Ocean) versus the east (Atlantic Ocean and Hudson Bay). We also identified subtle structure, not previously recognized, within Hudson Bay nesting common eiders. Our findings add to evidence linking wintering areas and genomic differentiation in waterfowl, offering further insights for management of this culturally important sea duck species.