The sensory bases of species and population mate preferences are well known; in frogs properties of the female auditory system influence such preferences. By contrast, there is little understanding of how sensory characteristics could result in sexual selection within a population. One possible mechanism is that females are more sensitive to male courtship signals that deviate from the population mean. We document this mechanism in the frog Physalaemus pustulosus. Female basilar papilla tuning is biased toward lower-than-average frequencies in the 'chuck' portion of the male's call, explaining female preference for the lower-frequency chucks produced by larger males. The tuning does not differ between P. pustulosus and its close relative P. coloradorum, a species in which males never evolved the ability to produce chucks; thus the female tuning evolved before the chuck and therefore the chuck played no role in the evolution of the preference. This allows us to reject two popular hypotheses for the evolution of this female preference (runaway sexual selection and natural selection) in favour of a third: sexual selection for sensory exploitation.