Salient cues, such as the rising sun or availability of food, entrain biological clocks for behavioral adaptation. The mechanisms underlying entrainment to food availability remain elusive. Using single-nucleus RNA sequencing during scheduled feeding, we identified a dorsomedial hypothalamus leptin receptor–expressing (DMH
LepR
) neuron population that up-regulates circadian entrainment genes and exhibits calcium activity before an anticipated meal. Exogenous leptin, silencing, or chemogenetic stimulation of DMH
LepR
neurons disrupts the development of molecular and behavioral food entrainment. Repetitive DMH
LepR
neuron activation leads to the partitioning of a secondary bout of circadian locomotor activity that is in phase with the stimulation and dependent on an intact suprachiasmatic nucleus (SCN). Last, we found a DMH
LepR
neuron subpopulation that projects to the SCN with the capacity to influence the phase of the circadian clock. This direct DMH
LepR
-SCN connection is well situated to integrate the metabolic and circadian systems, facilitating mealtime anticipation.