Aphid wing dimorphism is a textbook example of transgenerational phenotypic plasticity, but the signaling mechanism from mother to daughter remains unclear. We showed that the physical contact and crowding treatment caused high proportion of winged offspring in the pea aphid . RNA sequencing (RNA-seq) analysis indicated that the expression of brain () and embryonic () were increased by physical contact and crowding treatments. Knockdown of either gene inhibited phosphorylation of ApFoxO in embryos. Furthermore, electrophoretic mobility shift assays (EMSA) showed that dephosphorylated ApFoxO directly bound to the promotor of () to repress its transcription in stage 20 embryos, causing a lower winged proportion. Our results demonstrated that brain and embryonic coordinately relayed the maternal physical contact signals and control wing development in offspring, showcasing a regulatory mechanism underlying physical contact-dependent, transgenerational wing dimorphism in aphids.