Significance Juvenile hormone is unique to arthropods and controls numerous essential functions in these organisms. Its receptor, Methoprene-tolerant, turns on genes by directly binding to E-box–like motifs in their regulatory regions. However, how juvenile hormone represses genes has remained unclear. Here, we used the Aedes aegypti female mosquito, in which juvenile hormone is necessary for reproductive maturation, to show that the repressor Hairy is required for the gene-repressive action of juvenile hormone and Methoprene-tolerant. Moreover, we demonstrate that a corepressor, Groucho, supports this Hairy function. Hence, Methoprene-tolerant recruits the evolutionarily conserved Hairy/Groucho molecular system to mediate the juvenile hormone gene-repressive function.