While the origin of oligodendroglia in the prosencephalon and spinal cord has been extensively studied and accurately described, the origin of this cell type in the cerebellum is largely unknown. To investigate where cerebellar oligodendrocytes generate and which migratory pathways they follow to reach their final destination in the adult, in ovo transplants were performed using the quail/chick chimeric system. The chimeric embryos were developed up to HH43-49 (17–19 days of incubation) to map the location of donor cells and analyze their phenotype by immunohistochemistry. As a result, mesencephalic homotopic and homochronic transplants generated cellular migratory streams moving from the grafted epithelium into the host cerebellum, crossing the isthmus mainly through the velum medullare and invading the central white matter. From here, these mesencephalic cells invaded all the layers of the cerebellar cortex except the granular layer. The majority of the cells were detected in the central and folial white matter, as well as in superficial regions of the internal granular layer, surrounding the Purkinje cells. In the latter case, the donor cells presented a Bergmann glial morphology and were Vimentin positive, while in other areas they were PLP and Olig2-positive, indicating an oligodendroglial fate. The combinatory analysis of the different grafts allowed us to propose the fate map of chick cerebellar oligodendroglia at the neural tube stage. As a result, the majority of the cerebellar oligodendrocytes originate from the parabasal plate of the mesencephalon. © 2011 Wiley-Liss, Inc.