Adipokinetic hormones (AKHs) induce mobilization of energy reserves in insects, acting thus analogously to the human hormone glucagon. Experiments in the model insect Drosophila melanogaster have recently shown that loss of AKH results in adulthood-specific onset of obesity coupled with hypoglycemia. Nevertheless, not much is known about the exact mechanism whereby AKH affects fly physiology. Therefore, we investigated the physiological roles of this hormone, focusing on the metabolic rate and food intake control, and on the interactions between AKH and other fly neuropeptides known to regulate metabolism. Our gain- and loss-of-function experiments show that despite its anti-obesity effect, AKH is an orexigenic peptide. This hormone also affects expression of several other neuropeptide genes involved in feeding behavior, including orexigenic neuropeptides CCHamide-2 and neuropeptide F. In addition, AKH affects metabolic regulators like corazonin, limostatin, and insulin-like peptides 2, 3, 5 and 6. Altogether, our work shows that next to the regulation of the feeding behavior and metabolic rate, AKH signaling controls Drosophila metabolism also by affecting metabolic regulators from the family of insect neuropeptides. AKH should be thus viewed as a central regulator of energy homeostasis and neuroendocrine signaling in Drosophila adults.