Echolocation, the detection of objects by means of sound waves, has evolved independently in diverse animal lineages. Echolocating lineages include not only mammals such as toothed whales, yangochiropteran and rhinolophoid bats, but also Rousettus fruit bats, as well as two bird lineages, the oilbirds and swiftlets, which use echolocation to navigate in caves where they roost. In whales, yangochiropteran and rhinolophoid bats, positive selection and molecular convergence has been documented in key hearing-related genes, such as prestin (SLC26A5), but few studies have examined these loci in other echolocators. Here, we examine patterns of selection and convergence in echolocation-related genes in echolocating birds and Rousettus bats. Fewer of these loci were under selection in Rousettus or birds compared with classically-recognized echolocators, and elevated convergence (compared to background lineages) was not evident across this gene set. In certain genes, however, we detected convergent substitutions with potential functional relevance, including convergence between Rousettus and classic echolocators in prestin at a site known to affect hair cell electromotility. We also detected convergence between Yangochiroptera, Rhinolophidea and oilbirds in TMC1, an important mechanosensory transduction channel in vertebrate hair cells, and observed an amino acid change at the same site within the pore domain. Our results suggest that although most proteins implicated in echolocation in specialized mammals may not have been recruited in birds or Rousettus fruit bats, certain hearing-related loci may have undergone convergent functional changes. Investigating adaptations in diverse echolocators such as swiftlets and oilbirds will deepen our understanding of this unusual sensory modality.