The cerebrovascular network and its mural cells must meet the dynamic energy demands of different neuronal cell types across the brain, but their spatial relationship among these cells is largely unknown. Here, we apply brain-wide mapping methods to create a comprehensive cellular-resolution resource comprising the distribution of and quantitative relationship between microvessels, pericytes, and glutamatergic and GABAergic neurons including neuronal nitric oxide synthase-positive (nNOS+) neurons and their subtypes in mice. Leveraging these data, we discovered region-specific signatures of vasculature and cell type compositions across cortical and subcortical areas, including strikingly contrasting correlations between the density of vasculature, pericytes, glutamatergic neurons and parvalbumin-positive interneurons versus nNOS+ neurons in the isocortex. We also found surprisingly low vasculature and pericyte density in the hippocampus, and distinctly high pericyte to vasculature ratio in the hypothalamus. These findings suggest that vascular density and mural cell composition is finely tuned to maintain regional energy homeostasis.