In postnatal rodent brain, certain NG2-expressing oligodendroglial precursor cells (OPCs) are contacted by synaptic terminals from local neurons. However, it has remained elusive whether and when NG2⁺ cells are integrated into neuronal circuits. Here we use patch-clamp recordings from mitotic cells in murine brain slices to show that, unlike any other cell in the central nervous system (CNS), cortical NG2⁺ cells divide and relocate while being linked to synaptic junctions. Together with bromodeoxyuridine (BrdU) labeling, our recordings imply that cellular processes that bear synaptic junctions are surprisingly kept during cytokinesis and are inherited by the daughter cells. Cell cycle time (78 h) and relocation speed (5 µm/day) are slowed, and NG2⁺ cells largely divide symmetrically. Inheritance of synapses enables newborn glial cells to establish synaptic connections much faster than newborn neurons and ensures that the entire population of NG2⁺ cells is exposed to synaptic signals from local axons. The results suggest that synapses do not only transmit neuronal activity but also act as environmental cues for the development of glial cells. Inheritance of synapses allows for the direct transfer of environmental interactions to clonal descendants of OPCs, which might be important for effective colonization and myelination of the developing brain.—Kukley, M., Kiladze, M., Tognatta, R., Hans, M., Swandulla, D., Schramm, J., Dietrich, D. Glial cells are born with synapses.