The brain must guide immediate responses to beneficial and harmful stimuli while simultaneously writing memories for future reference. Both immediate actions and reinforcement learning are instructed by dopamine. However, it is unknown how dopaminergic systems maintain coherence between these two reward functions. Optogenetic activation experiments showed that the dopamine neurons that inform olfactory memory inDrosophilahave a distinct, parallel function driving attraction and aversion (valence). Olfactory-memory neurons were dispensable for valence. A broadly projecting set of dopaminergic cells had valence that was dependent on dopamine, glutamate, and octopamine. Similarly, a more restricted dopaminergic cluster with attractive valence was reliant on dopamine and glutamate. Opto-inhibition of this narrow subset revealed that behavior was influenced by pre-existing dopaminergic activity. Dopamine's acute effect on valence provides a mechanism by which a dopaminergic circuit can coherently write memories to influence future responses while guiding immediate actions.