Sexual signal evolution may present fitness consequences for the non‐signaling sex due to shared genes and altered social conditions, but this is rarely studied in natural populations. On the Hawaiian Island of Kauai, most male Teleogryllus oceanicus (Pacific field crickets) lack the ability to sing because of a novel wing mutation (flatwing) that arose and spread in <20 generations. Obligately silent flatwing males have been highly successful because they avoid detection by a deadly, acoustically‐orienting parasitoid fly. Little is known about how the flatwing mutation and resulting song‐less acoustic environment affects female fitness. We found that Kauai females carrying the flatwing allele invested less in reproductive tissues and experienced more instances of mating failure than normal‐wing‐carrying females, though total offspring production did not differ between female genotypes. Females from Oahu (HI, where the parasitoid and flatwing also occur) and Mangaia (an island in the Cook Islands which harbors neither the parasitoid nor flatwing) invested less in reproductive tissues when reared in a song‐less acoustic environment. Kauai females did not exhibit this plasticity, perhaps because they have experienced nearly song‐less conditions for the past ~15 years following the establishment of flatwing. We show that female T. oceanicus experience a mix of costly and beneficial effects of sexual signal loss, which should help maintain the wing polymorphism in the wild. Our results demonstrate that the non‐signaling sex can experience a nuanced set of phenotypic consequences resulting from signal evolution, which can further shape dynamics of sexual signal evolution.

How populations adapt, or not, to rapid evolution of sexual signals has important implications for population viability, but is difficult to assess due to the paucity of examples of sexual signals evolving in real time. In Hawaiian populations of the Pacific field cricket (Teleogryllus oceanicus), selection from a deadly parasitoid fly has driven the rapid loss of a male acoustic signal, calling song, that females use to locate and evaluate potential mates. In this newly quiet environment where many males are obligately silent, how do phonotactic females find mates? Previous work has shown that the acoustic rearing environment (presence or absence of male calling song) during late juvenile stages and early adulthood exposes adaptive flexibility in locomotor behaviors of males, as well as mating behaviors in both sexes that helps facilitate the spread of silent (flatwing) males. Here, we tested whether females also show acoustically induced plasticity in walking behaviors using laboratory‐reared populations of T. oceanicus from Kauai (HI; >90% flatwings), Oahu (HI; ~50% flatwings), and Mangaia (Cook Islands; no flatwings or parasitoid fly). Though we predicted that females reared without song exposure would increase walking behaviors to facilitate mate localization when song is rare, we discovered that, unlike males, female T. oceanicus showed relatively little plasticity in exploratory behaviors in response to an acoustic rearing environment. Across all three populations, exposure to male calling song during development did not affect latency to begin walking, distance walked, or general activity of female crickets. However, females reared in the absence of song walked slower and showed a marginally non‐significant tendency to walk for longer durations of time in a novel environment than those reared in the presence of song. Overall, plasticity in female walking behaviors appears unlikely to have facilitated sexual signal loss in this species.