Pine and oak woodlands are common North American floral communities with distinct regional species composition. The white-breasted nuthatch (Aves: Sitta carolinensis) is a common resident bird of North American pine and oak woodlands, and is distributed continentally across the highly disjunct distribution of these woodlands. We propose three historical hypotheses to explain the evolution of the white-breasted nuthatch in its principal habitat. (i) The species evolved in situ in the regional pine-oak communities and the isolation of populations in these regions is captured in cryptic genetic variation. (ii) Migration of individuals between regions is frequent enough to maintain the widespread distributions and prevent regional divergence. (iii) The species have recently expanded to occupy their current distributions and an insufficient amount of time has passed for divergence to occur. Phylogenetic analysis of mitochondrial DNA (ND2 gene) variation (N = 216) in the white-breasted nuthatch reveals four reciprocally monophyletic clades concordant with the distribution of the regional North American pine and oak woodlands, and supports hypothesis 1 of in situ evolution of populations in the regional pine and oak communities. Within-clade population structure and demographic history are also discussed.