Background: Metabolic activity and environmental energy are two of the most studied putative drivers of molecular evolutionary rates. Their extensive study, however, has resulted in mixed results and has rarely included the exploration of interactions among various factors impacting molecular evolutionary rates across large clades. Taking the diverse avian family Furnariidae as a case study, we examined the association between several estimates of molecular evolutionary rates with proxies of metabolic demands imposed by flight (wing loading and wing shape) and proxies of environmental energy across the geographic ranges of species (temperature and UV radiation). Results: We found weak evidence of a positive effect of environmental and morphological variables on mitochondrial substitution rates. Additionally, we found that temperature and UV radiation interact to explain molecular rates at nucleotide sites affected by selection and population size (non-synonymous substitutions), contrary to the expectation of their impact on sites associated with mutation rates (synonymous substitutions). We also found a negative interaction between wing shape (as described by the hand-wing index) and body mass explaining mitochondrial molecular rates, suggesting molecular signatures of positive selection or reduced population sizes in small-bodied species with greater flight activity. Conclusions: Our results suggest that the demands of flight and environmental energy pose multiple evolutionary pressures on the genome either by driving mutation rates or via their association with natural selection or population size. Data from whole genomes and detailed physiology across taxa will bring a more complete picture of the impact of metabolism, population size, and the environment on avian genome evolution.