The loss of sexual ornaments is observed across taxa, and pleiotropic effects of such losses provide an opportunity to gain insight into underlying dynamics of sex-biased gene expression and intralocus sexual conflict (IASC). We investigated this in a Hawaiian field cricket, Teleogryllus oceanicus, in which an X-linked genotype (flatwing) feminises males’ wings and eliminates their ability to produce sexually selected songs. We profiled adult gene expression across somatic and reproductive tissues of both sexes. Despite the feminising effect of flatwing on male wings, we found no evidence of feminised gene expression in males. Instead, female transcriptomes were more strongly affected by flatwing than males’, and exhibited demasculinised gene expression. These findings are consistent with a relaxation of IASC constraining female gene expression through loss of a male sexual ornament. In a follow-up experiment we found reduced testes mass in flatwing males, whereas female carriers showed no reduction in egg production. In contrast, female carriers exhibited greater measures of body condition. Our results suggest sex-limited phenotypic expression offers only partial resolution to intralocus sexual conflict, owing to pleiotropic effects of the loci involved. Benefits conferred by release from intralocus conflict could help explain widespread loss of sexual ornaments across taxa.