The theory of ecological speciation posits that adaptive divergence among incipient species raises incidental barriers to reproduction, thus catalyzing the emergence of new species. In this study, we conducted an experimental test of this theory in Galápagos finches, a clade in which beaks and mating songs are mechanistically linked. We forecasted the acoustic structure of songs for a set of possible evolutionary futures (successive droughts spurring increasingly large beaks) and, in a field assay, presented resulting song simulations to territorial males. We found that responses to songs dropped off after six simulated drought events, to degrees roughly comparable to drops in response to songs that diverged through cultural drift and acoustic adaptation. Our results support, in Darwin’s finches, the feasibility and mechanistic bases of an ecological speciation hypothesis.