<p>Changes in host carbohydrate metabolism determine the outcome of host–parasite relationships, but the underlying mechanistic basis remains elusive. Here, we show that the parasitoid wasp <i>Cotesia vestalis</i> induces trehalose accumulation in its host, the moth <i>Plutella xylostella</i>, largely independently of insulin/adipokinetic hormone signalling and food intake. Instead, parasitoids rewire host carbohydrate metabolism via two pathways activated by the evolutionarily conserved short neuropeptide F (sNPF), a functional analogue of mammalian neuropeptide Y. Parasitoid-derived teratocytes secrete sNPF that interacts with the sNPF receptor (sNPFR) on host cells, and contributes to host hypertrehalosemia by promoting glycogenolysis in the fat body. We further find that a parasitoid-symbiotic virus induces expression of host-encoded sNPF, which stimulates glycolysis in the host midgut. Furthermore, we show that the host sNPF-sNPFR complex stimulates G_q/Ca²⁺ signalling, while the parasitoid sNPF, exhibiting higher receptor affinity, triggers G_i/cAMP signalling. Molecular docking analyses suggest that the observed distinct receptor activation properties may be attributed to structural variations in the sNPF-sNPFR binding pocket. Collectively, our findings uncover an unexpected role of peripheral sNPFs in the regulation of carbohydrate metabolism during host–parasite interactions.</p>