Obesity is primarily a consequence of consuming calories beyond energetic requirements, but underpinning drivers have not been fully defined. 5-Hydroxytryptamine (5-HT) neurons in the dorsal Raphe nucleus (5-HT) regulate different types of feeding behavior, such as eating to cope with hunger or for pleasure. Here, we observed that activation of 5-HT to hypothalamic arcuate nucleus (5-HT → ARH) projections inhibits food intake driven by hunger via actions at ARH 5-HT and 5-HT receptors, whereas activation of 5-HT to ventral tegmental area (5-HT → VTA) projections inhibits non-hunger-driven feeding via actions at 5-HT receptors. Further, hunger-driven feeding gradually activates ARH-projecting 5-HT neurons via inhibiting their responsiveness to inhibitory GABAergic inputs; non-hunger-driven feeding activates VTA-projecting 5-HT neurons through reducing a potassium outward current. Thus, our results support a model whereby parallel circuits modulate feeding behavior either in response to hunger or to hunger-independent cues.