Neuronal identities are resolved postmitotically as newly born cells acquire distinct molecular programs, migratory trajectories, and anatomical destinations. This process is especially apparent in the lateral and caudal ganglionic eminences, whose precursors generate interneurons destined for the olfactory bulb, hippocampus, and cortex. How postmitotic programs distinguish among these identities and destinations remains unresolved. Here, we show that Prox1 directs the positioning and identity of CGE-derived cortical and hippocampal interneurons. Prox1 specifies VIP, LAMP5, and SNCG cortical and hippocampal identities, whereas its absence permits the emergence of CGE-derived NTNG1 and SNCG hippocampus-specific interneurons, as well as LGE-derived olfactory bulb interneurons. Removal of Prox1 converts prospective cortical CGE interneurons toward these alternative fates, while ectopic Prox1 in LGE precursors redirects cells toward the prefrontal cortex. In macaque, this same program is redeployed in LGE-derived interneurons migrating to the cortex. These findings suggest that evolutionary changes in interneuron allocation can arise through reuse of conserved postmitotic programs.