Gammapolyomaviruses may cause serious inflammatory diseases in a broad range of avian hosts. In this study we investigated genomic evolution of and selection constraint acting on avian polyomaviruses (APyVs). Our analyses suggested that goose haemorrhagic polyomavirus (GHPV) evolves more slowly (3.03 × 10-5 s/s/y mean evolutionary rate) than budgerigar fledgling disease virus (BFDV), finch polyomavirus (FPyV) and canary polyomavirus (CaPyV) (1.39 × 10-4 s/s/y, 2.63 × 10-4 s/s/y and 1.41 × 10-4 s/s/y mean evolutionary rate, respectively). In general, purifying selection seems to act on the protein coding regions of APyV genomes, although positive Darwinian selection was also predicted in a few positions (e.g., in the large tumor antigen coding region of BFDV and GHPV and in the capsid protein sequences of BFDV). The importance of these aa changes remains elusive. Overall, a better understanding of adaptive changes in the genome of APyVs requires additional data from various incidental hosts and reservoir species.