Finding food and remaining at a food source are crucial survival strategies. We show how neural circuits and signaling molecules regulate these food-related behaviors in Caenorhabditis elegans. In the absence of food, AVK interneurons release FLP-1 neuropeptides that inhibit motorneurons to regulate body posture and velocity, thereby promoting dispersal. Conversely, AVK photoinhibition promoted dwelling behavior. We identified FLP-1 receptors required for these effects in distinct motoneurons. The DVA interneuron antagonizes signaling from AVK by releasing cholecystokinin-like neuropeptides that potentiate cholinergic neurons, in response to dopaminergic neurons that sense food. Dopamine also acts directly on AVK via an inhibitory dopamine receptor. Both AVK and DVA couple to head motoneurons by electrical and chemical synapses to orchestrate either dispersal or dwelling behavior, thus integrating environmental and proprioceptive signals. Dopaminergic regulation of food-related behavior, via similar neuropeptides, may be conserved in mammals. Display omitted •Presence or absence of food promotes the dwelling or dispersal behavior of C. elegans•Dopamine signals to peptidergic interneurons in response to food•Peptidergic interneurons antagonize each other to inhibit or excite motoneurons•Cholecystokinin and RFamide modulate motoneurons to generate food response behavior In this study of C. elegans food response behavior, the underlying circuitry is identified by dopaminergic neurons signaling the presence of food to interneurons that release neuropeptides and regulate locomotion by conferring distinct motoneuron responses via specific neuropeptide receptor expression.