Environmental stimuli experienced by the parental generation influence the phenotype of subsequent generations. The effects of these stimuli on the parental generation may be passed through the germline, but the mechanisms of this non-Mendelian type of inheritance are poorly known. Here we show that modulation of nutrient-sensing pathways in the parental generation of a nematode (Auanema freiburgensis) regulates phenotypic plasticity of its offspring. In response to pheromones, AMP-activated protein kinase (AMPK), mechanistic target of rapamycin complex 1 (mTORC1) and insulin signaling regulate stress resistance and sex determination across a generation. The effectors of these pathways are closely associated with the chromatin and their regulation affects the acetylation chromatin status in the germline. These results suggest that highly conserved metabolic sensors regulate phenotypic plasticity by changing the epigenetic status of the germline.