While the CNSs of the chordate sister clades Tunicata and Vertebrata have unmistakable homology, the extent of their conservation is still being uncovered. We report that the hindbrain of the tunicate Ciona, like those of vertebrates, has functionally-distinct dorsal and ventral domains. The Ciona dorsal hindbrain functions as a relay and processing center for peripheral sensory neurons, while in vertebrates the dorsal hindbrain forms the cerebellum. Despite the different fates of dorsal hindbrains in Ciona versus vertebrates, we present evidence from analysis of gene expression, developmental mechanisms, and neural circuit architecture that they share a common origin. While it is generally agreed that the cerebellum evolved in vertebrates, our findings indicate that a dorsally-positioned precursor to the cerebellum has much deeper roots.