Convergence offers an opportunity to explore to what extent evolution can be predictable when genomic compositions and environmental triggers are similar. Here we present an emergent model system to study convergent evolution in nature in a mammalian group, the bat genus Myotis. Three foraging strategies – gleaning, trawling, and aerial hawking, each characterized by different sets of phenotypic features – have evolved independently multiple times in different biogeographic regions in isolation for millions of years. To investigate the genomic basis of convergence and explore the functional genomic changes linked to ecomorphological convergence, we sequenced and annotated 17 new genomes and screened 16,426 genes for positive selection and associations between relative evolutionary rates and foraging strategies across 30 bat species representing all Myotis ecomorphs across geographic regions as well as among sister groups. We identify genomic changes that describe both phylogenetic and ecomorphological trends. We infer that colonization of new environments may have first required changes in genes linked to hearing sensory perception, followed by changes linked to fecundity and development, metabolism of carbohydrates, and heme degradation. These changes may be linked to prey acquisition and digestion and match phylogenetic trends. Our findings also suggest that the repeated evolution of ecomorphs does not always involve changes in the same genes but rather in genes with the same molecular functions such as developmental and cellular processes.