Heteropatric differentiation is a mode of speciation with gene flow in which divergence occurs between lineages that are in sympatry and allopatry at different times during cyclic spatial movements. Empirical evidence suggests that heteropatric differentiation may prove to be common among seasonally migratory organisms. We examined genetic differentiation between the sedentary Aleutian Islands population of green-winged teal (Anas crecca nimia) and its close migratory relative, the Eurasian, or Old World (OW), Anas c. crecca population, a portion of which passes through the range of nimia during its seasonal migrations. We also examined its relationship with the parapatric North American, New World (NW), A. c. carolinensis population. Sequence data from eight nuclear introns and the mtDNA control region showed that the nimia-crecca divergence occurred much more recently than the deeper crecca-carolinensis split (~83,000 y vs. ~1.1 My). Despite considerable spatial overlap between crecca and nimia during seasonal migration, three key predictions of heteropatric differentiation are supported: significant genetic divergence (overall mean Φst = 0.07), low gene flow (2Nem ~1.8), and an effective population size in nimia that is not especially low (Ne ~ 80,000 individuals). Similar levels of gene flow have come into nimia from carolinensis, but no detectable nuclear gene flow has gone out of nimia into either OW (crecca) or NW (carolinensis) populations. We infer that adaptations of these populations to local optima in different places (e.g., each matching their reproductive effort to different resource blooms) promote genetic isolation and divergence despite periods of sympatry between them, as the heteropatric model predicts.