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.