With methods for sequencing thousands of loci for many individuals, phylogeographic studies have increased inferential power and the potential for applications to new questions. In songbirds, strong patterns of inter-chromosomal synteny, the published genome of a songbird and the ability to obtain thousands of genetic loci for many individuals permit the investigation of differentiation between and diversity within lineages across chromosomes. Here, we investigate patterns of differentiation and diversity in Certhia americana, a widespread North American songbird, using next-generation sequencing. Additionally, we reassess previous phylogeographic studies within the group. Based on ~ 30 million sequencing reads and more than 16 000 single-nucleotide polymorphisms in 41 individuals, we identified a strong positive relationship between genetic differentiation and chromosome size, with a negative relationship between genetic diversity and chromosome size. A combination of selection and drift may explain these patterns, although we found no evidence for selection. Because the observed genomic patterns are very similar between widespread, allopatric clades, it is unlikely that selective pressures would be so similar across such different ecological conditions. Alternatively, the accumulation of fixed differences between lineages and loss of genetic variation within lineages due to genetic drift alone may explain the observed patterns. Due to relatively higher recombination rates on smaller chromosomes, larger chromosomes would, on average, accumulate fixed differences between lineages and lose genetic variation within lineages faster, leading to the patterns observed here in C. americana.