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Cuticular proteins (CPs) are major components of the insect cuticle-associated organs such as integument and wings, although the importance of CPs for wing development and function in hemimetabolous insects remains understudied. In the present study, a wing cuticular protein LmACP8 was identified from Locusta migratoria , which belongs to the RR-2 subfamily of cuticular protein R&R consensus (CPR) chitin-binding proteins. LmACP8 was mainly expressed in the wing pads and showed high expression levels before ecdysis of third-, fourth-, and fifth-instar nymphs, with its encoded protein located in the procuticle of wing pads and adult wings. Depletion of LmACP8 by RNA interference markedly reduced the amount of its protein, which consequently caused abnormal wing morphogenesis in the transition from nymph to adult of L.?migratoria. We further demonstrated that the abnormal morphogenesis was caused by severe damage of the endocuticle in the wings. LmACP8 was suppressed by 20-hydroxyecdysone (20E) in vivo, however, its expression was significantly up-regulated after knocking down the hormone receptor gene LmHR39 . Thus, the LmACP8 that is negatively regulated by the LmHR39-mediated 20E signaling pathway is involved in wing development during the nymph to adult transition.