Quantifying population genetic structure is fundamental to testing hypotheses regarding gene flow, population divergence and dynamics across large spatial scales. In species with highly mobile life-history stages, where it is unclear whether such movements translate into effective dispersal among discrete philopatric breeding populations, this approach can be particularly effective. We used seven nuclear microsatellite loci and mitochondrial DNA (ND2) markers to quantify population genetic structure and variation across 20 populations (447 individuals) of one such species, the European Shag, spanning a large geographical range. Despite high breeding philopatry, rare cross-sea movements and recognized subspecies, population genetic structure was weak across both microsatellites and mitochondrial markers. Furthermore, although isolation-by-distance was detected, microsatellite variation provided no evidence that open sea formed a complete barrier to effective dispersal. These data suggest that occasional long-distance, cross-sea movements translate into gene flow across a large spatial scale. Historical factors may also have shaped contemporary genetic structure: cluster analyses of microsatellite data identified three groups, comprising colonies at southern, mid- and northern latitudes, and similar structure was observed at mitochondrial loci. Only one private mitochondrial haplotype was found among subspecies, suggesting that this current taxonomic subdivision may not be mirrored by genetic isolation.