Parasitoids alter host energy homeostasis to create a favorable environment for their own development. However, the mechanisms underlying this process remain largely unexplored, especially for gregarious parasitoids. Cotesia ruficrus , a gregarious endoparasitoid native to China, targets the invasive pest Spodoptera frugiperda (fall armyworm, FAW) and has been shown to effectively control FAW populations. This study investigates the role of the polydnavirus (PDV) produced by C. ruficrus in regulating lipid metabolism of FAW larvae. The results demonstrated that, following PDV injection for 5 days, both triglyceride concentrations and lipid droplet diameters in the fat bodies of FAW larvae significantly increased. RNA interference (RNAi) targeting the PDV gene CrBV3–31 led to a reduction in triglyceride concentrations and lipid droplet size, along with an upregulation of the LSD1 gene. Furthermore, silencing CrBV3–31 decreased triglyceride levels in C. ruficrus pupae and lowered its eclosion rate. These findings suggest that the PDV gene CrBV3–31 plays a crucial role in enhancing lipid accumulation in FAW larvae, thereby supporting the survival of C. ruficrus offspring. This study uncovers a novel mechanism by which gregarious endoparasitoids exploit symbiotic bracovirus genes to regulate host energy metabolism, increasing lipid levels to meet the developmental needs of their multiple offspring.