In Drosophila, anatomically discrete dopamine neurons that innervate distinct zones of the mushroom body (MB) assign opposing valence to odors during olfactory learning. Subsets of MB neurons have temporally unique roles in memory processing, but valence-related organization has not been demonstrated. We functionally subdivided the alphabeta neurons, revealing a value-specific role for the approximately 160 alphabeta core (alphabetac) neurons. Blocking neurotransmission from alphabeta surface (alphabetas) neurons revealed a requirement during retrieval of aversive and appetitive memory, whereas blocking alphabetac only impaired appetitive memory. The alphabetac were also required to express memory in a differential aversive paradigm demonstrating a role in relative valuation and approach behavior. Strikingly, both reinforcing dopamine neurons and efferent pathways differentially innervate alphabetac and alphabetas in the MB lobes. We propose that conditioned approach requires pooling synaptic outputs from across the alphabeta ensemble but only from the alphabetas for conditioned aversion.