We found that demyelinated axons formed functional glutamatergic synapses onto adult-born NG2⁺ oligodendrocyte progenitor cells (OPCs) migrating from the subventricular zone after focal demyelination of adult mice corpus callosum. This glutamatergic input was substantially reduced compared with endogenous callosal OPCs 1 week after lesion and was lost on differentiation into oligodendrocytes. Therefore, axon–oligodendrocyte progenitor synapse formation is a transient and regulated step that occurs during remyelination of callosal axons.