An effective way to understand the genomics of divergence in non-model organisms is to use the transcriptome to identify genes associated with divergence. We examine the transcriptome of the song sparrow (Melospiza melodia) and contrast it with the avian models zebra finch (Taeniopygia guttata) and chicken (Gallus gallus). We aimed to (i) obtain a functional annotation of a substantial portion of the song sparrow transcriptome; (ii) compare transcript divergence; (iii) efficiently characterize single nucleotide polymorphism/indel markers possibly fixed between song sparrow subspecies; and (iv) identify the most common set of transcripts in birds using the zebra finch as a reference. Using two individuals from each of three populations, whole-body mRNA was normalized and sequenced (110 Mb total). The assembly yielded 38,539 contigs [N50 (the length-weighted median) = 482 bp]; 4574 were orthologous to both model genomes and 3680 are functionally annotated. This low-coverage scan of the song sparrow transcriptome revealed 29,982 SNPs/indels, 1402 fixed between populations and subspecies. Referencing zebra finch and chicken, we identified 43 and 5 fast-evolving genes, respectively. We also identified the most common set of transcripts present in birds with respect to zebra finch. This study provides new insight into songbird transcriptomes, and candidate markers identified here may help research in songbirds (oscine Passeriformes), a frequently studied group.