This study reveals a sexually dimorphic sNPF-sNPF-R circuit in the Drosophila brain that regulates energy balance behavior, specifically the shorter-mating-duration (SMD) response to sexual experience. sNPF is predominantly expressed in neurons, while sNPF-R is expressed in both neurons and glial cells, particularly astrocyte-like glia (ALG) in a subset of cells outside the mushroom body (MB) termed "Rishi cells" (RS cells). Sexual experience induces global alterations in calcium signaling and synaptic plasticity within this circuit, with sNPF-R expressing neurons and glia in RS cells playing a critical role in encoding sexual experience-related information into energy balance behavior related to mating duration. Neuronal glucose metabolism, specifically the Tret1l transporter, is essential for maintaining the high calcium levels and proper function of sNPF neurons near RS cells. This novel and intricate neuron-glia sNPF-sNPF-R network acts as critical circuits within the Drosophila brain for processing interval timing behaviors, highlighting the dynamic interplay between metabolism, neural circuits, and behavior in regulating energy balance.