Several different factors may determine where species range limits are located within regions of otherwise continuously available habitat and suitable climate. Within the Arctic tundra biome many bird species are migratory and their breeding distributions are affected by migration routes that are in turn limited by factors such as suitable winter habitat, migratory stopover sites, geographical barriers and historical routes of colonization. We identified longitudinal zones in the circumpolar Arctic of pronounced changes in the avian species composition (high species spatial turnover; 'species divides'). We tested for the association between migratory status and the geographical location and numbers of such species divides for species with non-breeding habitats mainly within terrestrial, pelagic and coastal ecosystems. Our results demonstrate that migration is of profound importance for both the number and locations of species divides in the Arctic. Long-distance migration is associated with a large number of divides among terrestrial and coastal arctic birds but with a reduced number of divides among pelagic birds. We suggest that long-distance migration permits pelagic but not terrestrial and coastal birds to colonize large winter ranges, which in turn causes expansion of breeding ranges, with more homogenous communities and reduction of species divides as consequences, among the long-distance migrants of pelagic but not of terrestrial and coastal birds. Furthermore, the divides among long-distance migrants are situated in two main regions, the Beringia and Greenland zones, while divides among short-distance migrants are more evenly spaced throughout the circumpolar Arctic. The Beringia and Greenland divides result largely from inter-continental colonization of new breeding ranges but retainment of original winter quarters in a process of evolution through extension of migration routes, leading to aggregated divides in the meeting zones of major global flyways.