There is growing interest in understanding patterns of seasonal migratory connectivity between breeding and wintering sites, both because differences in migratory behaviour can be associated with population differentiation and because knowledge of migratory connectivity is essential for understanding the ecology, evolution and conservation of migratory species. We present the first broad survey of geographic variation in the nuclear genome of breeding and wintering Wilson’s warblers (Wilsonia pusilla), which have previously served as a research system for the study of whether genetic markers and isotopes can reveal patterns of migratory connectivity. Using 153 samples surveyed at up to 257 variable amplified fragment length polymorphism markers, we show that Wilson’s warblers consist of highly distinct western and eastern breeding groups, with all winter samples grouping with the western breeding group. Within the west, there is weak geographic differentiation, at a level insufficient for use in the assignment of wintering samples to specific areas. The distinctiveness of western and eastern genetic groups, with no known intermediates, strongly suggests that these two groups are cryptic species. Analysis of mitochondrial cytochrome b sequence variation shows that the estimated coalescence time between western and eastern clades is approximately 2.3 Ma, a surprisingly old time of divergence that is more typical of distinct species than of subspecies. Given their morphological similarity but strong genetic differences, western and eastern Wilson’s warblers present a likely case of association between divergence in migratory behaviour and the process of speciation.