Adipokinetic hormone (AKH), an analog of mammalian glucagon, functions in supplying the required energy by releasing lipids and carbohydrates from the fat body into the hemolymph. Our previous study showed that AKH receptor (AKHR) knockdown in the two-spotted cricket Gryllus bimaculatus decreased hemolymph lipid levels and increased its feeding frequency. To reveal underlying mechanisms by which AKH signaling modulates lipid homeostasis, we analyzed the fatty acid composition as the lipid structure in the crickets. AKH administration significantly increased the proportion of unsaturated fatty acids (USFAs) to total fatty acids with decrease of the saturated fatty acids (SFAs) in hemolymph, while these proportions were inversely changed in RNA interference-mediated AKHR-knockdowned (AKHRRNAi) crickets. Interestingly, knockdown of hormone-sensitive lipase (Hsl) by RNAi (HslRNAi) affected the proportion of USFAs and SFAs in a similar manner to that observed in AKHRRNAi crickets. AKH administration in HslRNAi crickets did not change hemolymph fatty acid composition, indicating that AKH signaling critically altered fatty acid composition in the hemolymph through Hsl. In addition, a choice assay revealed that AKHRRNAi significantly increases the preference of USFAs. These data indicate that hemolymph lipid level and composition were modulated by AKH signaling with a complementary feeding behavior toward USFAs.