To understand the cellular composition and region-specific specialization of white matter — a disease-relevant, glia-rich tissue highly expanded in primates relative to rodents — we profiled transcriptomes of ~500,000 nuclei from 19 tissue types of the central nervous system of healthy common marmoset and mapped 87 subclusters spatially onto a 3D MRI atlas. We performed cross-species comparison, explored regulatory pathways, modeled regional intercellular communication, and surveyed cellular determinants of neurological disorders. Here, we analyze this resource and find strong spatial segregation of microglia, oligodendrocyte progenitor cells, and astrocytes. White matter glia are diverse, enriched with genes involved in stimulus-response and biomolecule modification, and predicted to interact with other resident cells more extensively than their gray matter counterparts. Conversely, gray matter glia preserve the expression of neural tube patterning genes into adulthood and share six transcription factors that restrict transcriptome complexity. A companion Callithrix jacchus Primate Cell Atlas (CjPCA) is available through https://cjpca.ninds.nih.gov.