Myelin formation during development and remyelination following injury is a tightly regulated process that is not well understood. The orphan G protein-coupled receptor Gpr62, which is enriched in mature myelinating oligodendrocytes, has previously been shown to be unnecessary in developmental myelination. Here, we show that Gpr62 is a regulator of process formation in remyelination by the Gli1-expressing neural stem cells from the subventricular zone of the adult mouse brain. Additionally, we demonstrate that Gpr62 signals through the cAMP pathway to downregulate oligodendrocyte maturation.