High-throughput single-cell omics of non-human primate (NHP) brain tissue provide a powerful opportunity to investigate the molecular basis of brain aging. Here, we present a comprehensive transcriptomic and chromatin accessibility atlas comprising 2,955,873 cells from eight brain regions of 23 female cynomolgus macaques spanning the adult lifespan, including exceptionally old individuals. Our analyses reveal dynamic age-related molecular changes in core brain functions, including synaptic communication and axon myelination, with pronounced cell-type- and region-specific patterns. We further identify multicellular networks in the pons and medulla as a previously unrecognized hotspot of brain aging. Meta-analyses integrating human brain aging and neurodegeneration datasets uncover both shared and distinct molecular mechanisms underlying primate brain aging and disease. Finally, we identify transcription factors and age-related chromatin remodeling linked to longevity and neurodegeneration. Together, this spatiotemporal atlas constitutes a valuable resource for advancing our understanding of primate brain aging and its implications for health and disease.