Maternal behaviors are essential for the survival of the young. Previous studies implicated the medial preoptic area (MPOA) as an important region for maternal behaviors, but details of the maternal circuit remain incompletely understood. Here we identify estrogen receptor alpha (Esr1)-expressing cells in the MPOA as key mediators of pup approach and retrieval. Reversible inactivation of MPOAEsr1+ cells impairs those behaviors, whereas optogenetic activation induces immediate pup retrieval. In vivo recordings demonstrate preferential activation of MPOAEsr1+ cells during maternal behaviors and changes in MPOA cell responses across reproductive states. Furthermore, channelrhodopsin-assisted circuit mapping reveals a strong inhibitory projection from MPOAEsr1+ cells to ventral tegmental area (VTA) non-dopaminergic cells. Pathway-specific manipulations reveal that this projection is essential for driving pup approach and retrieval and that VTA dopaminergic cells are reliably activated during those behaviors. Altogether, this study provides new insight into the neural circuit that generates maternal behaviors. Display omitted •MPOAEsr1+ cells are necessary and sufficient for driving pup approach and retrieval•MPOAEsr1+ cells are naturally and preferentially activated during pup retrieval•MPOA cells decrease baseline firing and increase response to pups during lactation•MPOAEsr1+ provides strong inhibitory inputs to VTA non-DA cells to drive retrieval Maternal behavior is mediated by a hardwired neural circuit that remains poorly understood. Fang et al. find that medial preoptic Esr1+ cells (MPOAESR1+) are highly active during maternal behaviors. Activation of MPOAESR1+ projection to ventral tegmental area drives immediate pup retrieval.