The dorsal midline of the vertebrate neural tube is a source of signals that direct cell fate specification and proliferation. Using genetic fate mapping in the mouse and a previously generated Wnt3aCre line, we report here that genetically labeled cells of the Wnt3a lineage migrate widely from the dorsal midline into the dorsal half of the adult brain and spinal cord, contributing to diverse structures in the diencephalon, midbrain, and brainstem and extensively populating the rostral spinal cord. Conspicuously, many of these structures are linked in specific functional networks. Wnt3a lineage cells populate nuclei of the central auditory system from the medulla to thalamus, and the trigeminal sensory system from the cervical spinal cord to the midbrain. Our findings reveal the rich contributions of the Wnt3a lineage to a variety of brain structures and show that functionally integrated nuclei can share a molecular identity, provided by transient gene expression early in their development.