The relative contributions of past and present evolutionary processes in shaping population genetic differentiation can be difficult to ascertain, especially in highly mobile animals. The Northern Gannet (Morus bassanus; hereafter, gannet) is a migratory colonial seabird that is widely distributed across the North Atlantic Ocean. Despite strong dispersal abilities, decades of banding and tracking studies indicate that the North Atlantic is a barrier for seasonal migration of gannets: gannets breeding in North America winter along the southeastern coast of USA and Mexico, while European breeders winter along the western European and African coasts. However, telemetry recently revealed that some gannets migrate across the ocean, suggesting that trans-Atlantic gene flow is possible. We investigated patterns of genomic variation among gannets from 12 colonies across the species’ range using double digest restriction-site associated sequencing (ddRADseq). Indices of genetic differentiation, principal component analysis, a Bayesian clustering method, and discriminant analysis of principal components all indicated that gannets breeding in North America versus Europe differ genetically, in accordance with segregation at both breeding and non-breeding areas. However, Bayesian assignment methods indicated that low, unidirectional introgression occurs from Europe into North America, suggesting that the North Atlantic is a semi-permeable barrier to gene flow in gannets. Evolutionary modeling suggested that the two genetic populations originated in separate refugia during the Pleistocene and underwent secondary contact during the Holocene. These results are consistent with results of previous studies and provide direct evidence that seasonal migratory behaviour can influence population genetic structure in a highly mobile organism.