Comparative studies of linguistic faculties in animals pose an evolutionary paradox: language involves certain perceptual and motor abilities, but it is not clear that this serves as more than an input–output channel for the externalization of language proper. Strikingly, the capability for auditory–vocal learning is not shared with our closest relatives, the apes, but is present in such remotely related groups as songbirds and marine mammals. There is increasing evidence for behavioral, neural, and genetic similarities between speech acquisition and birdsong learning. At the same time, researchers have applied formal linguistic analysis to the vocalizations of both primates and songbirds. What have all these studies taught us about the evolution of language? Is the comparative study of an apparently species-specific trait like language feasible? We argue that comparative analysis remains an important method for the evolutionary reconstruction and causal analysis of the mechanisms underlying language. On the one hand, common descent has been important in the evolution of the brain, such that avian and mammalian brains may be largely homologous, particularly in the case of brain regions involved in auditory perception, vocalization, and auditory memory. On the other hand, there has been convergent evolution of the capacity for auditory–vocal learning, and possibly for structuring of external vocalizations, such that apes lack the abilities that are shared between songbirds and humans. However, significant limitations to this comparative analysis remain. While all birdsong may be classified in terms of a particularly simple kind of concatenation system, the regular languages, there is no compelling evidence to date that birdsong matches the characteristic syntactic complexity of human language, arising from the composition of smaller forms like words and phrases into larger ones.