The rise and fall of a motivational state can unfold over many days. We used mouse mating behavior to model how the brain orchestrates such slow-timescale changes in motivation. Male mice become sexually satiated after successful matings, and their motivation to mate recovers over a week. Using deep-brain fluorescence-lifetime imaging in the medial preoptic area (MPOA), we found that tonic dopamine transmission-which regulates mating drive-also declined after mating and gradually re-emerged across several days. Two mechanisms regulated dopamine transmission. First, successful mating transiently reduced the tonic firing of hypothalamic dopamine-releasing neurons, thereby inhibiting dopamine release and mating behavior for 1 to 2 days. Second, these neurons' ability to produce and release dopamine dropped after mating and recovered over the following week, paralleling the recovery of mating drive. Therefore, changes in neuronal firing rate and neurotransmitter composition cooperate to control the early and late phases of motivational dynamics, respectively.