Natural systems composed of closely-related taxa that vary in the degree of phenotypic divergence and geographic isolation, provide an opportunity to investigate the rate of phenotypic diversification and the relative roles of selection and drift in driving lineage formation. The genus Junco (Aves: Emberizidae) of North America includes parapatric northern forms that are markedly divergent in plumage pattern and color, in contrast to geographically isolated southern populations in remote areas that show moderate phenotypic divergence. Here, we quantify patterns of phenotypic divergence in morphology and plumage color, and use mitochondrial DNA genes, a nuclear intron, and genome-wide SNPs to reconstruct the demographic and evolutionary history of the genus to infer relative rates of evolutionary divergence among lineages. We found that geographically isolated populations have evolved independently for hundreds of thousands of years despite little differentiation in phenotype, in sharp contrast to phenotypically diverse northern forms, which have diversified within the last few thousand years as a result of the rapid postglacial recolonization of North America. SNP data resolved young northern lineages into reciprocally monophyletic lineages, indicating low rates of gene flow even among closely related parapatric forms, and suggesting a role for strong genetic drift or multifarious selection acting on multiple loci in driving lineage divergence. Juncos represent a compelling example of speciation-in-action, where the combined effects of historical and selective factors have produced one of the fastest cases of speciation known in vertebrates.