Populations that have experienced long periods of geographic isolation will diverge over time. The application of high-throughput sequencing technologies to study the genomes of related taxa now allows us to quantify, at a fine scale, the consequences of this divergence across the genome. Throughout a number of studies, a notable pattern has emerged. In many cases, estimates of differentiation across the genome are strongly heterogeneous; however, the evolutionary processes driving this striking pattern are still unclear. Here we quantified genomic variation across several groups within the Yellow-rumped Warbler species complex (Setophaga spp.), a group of North and Central American wood warblers. We showed that genomic variation is highly heterogeneous between some taxa and that these regions of high differentiation are relatively small compared to those in other study systems. We found that the clusters of highly differentiated markers between taxa occur in gene-rich regions of the genome and exhibit low within-population diversity. We suggest these patterns are consistent with selection, shaping genomic divergence in similar genomic regions across the different populations. Our study also confirms previous results relying on fewer genetic markers that several of the phenotypically distinct groups in the system are also genomically highly differentiated, likely to the point of full species status.