Developmental myelination is a protracted process in the mammalian brain. One theory for why oligodendrocytes mature so slowly posits that myelination may stabilize neuronal circuits and temper neuronal plasticity as animals age. We tested this theory in the visual cortex, which has a well-defined critical period for experience-dependent neuronal plasticity. During adolescence, visual experience modulated oligodendrocyte maturation in visual cortex. To determine whether oligodendrocyte maturation in turn regulates neuronal plasticity, we genetically blocked oligodendrocyte differentiation and myelination in adolescent mice. In adult control mice, visual cortex activity following monocular deprivation remained stable, as expected for post-critical period animals. By contrast, visual cortex responses to the deprived eye decreased significantly in mice with impaired adolescent oligodendrogenesis, reminiscent of the plasticity normally restricted to adolescent mice. Furthermore, visual cortex neurons in mice lacking adolescent oligodendrogenesis had fewer dendritic spines, a higher level of spine turnover, and exhibited spatially coordinated spine size decreases following monocular deprivation. These results establish a critical role for oligodendrocytes in shaping the maturation and stabilization of cortical circuits and support the concept of myelin acting as a brake on neuronal plasticity during development.