This study reveals the genomic architecture of a rapidly evolving mutation which segregates as a single-locus, X-linked trait -- flatwing -- in wild Hawaiian field crickets (Teleogryllus oceanicus). Flatwingsilences males by eliminating sound-producing structures on their forewings. Silence protects them from an acoustically-orienting parasitoid fly (Ormia ochracea), but interferes with their ability to attract and court females for mating. Silent crickets spread rapidly on several Hawaiian islands under pressure from the flies, representing one of the fastest rates of evoutionary change documented in the wild. Here we present an annotated genome sequence of T. oceanicus along with a linkage map and QTL analysis of the trait derived from RAD-sequencing of a backcrossed mapping population. RNA-seq was used to probe the functional pathways affected by the mutation during early development, and pleiotropic effects on another signaling trait, cuticular hydrocarbons, were assessed and genetically mapped.