The supply of blood to brain tissue is thought to depend on the overall neural activity in that tissue, and this dependence is thought to differ across brain regions and across levels of arousal. Studies supporting these views, however, measured neural activity as a bulk quantity, and related it to blood supply following disparate events in different regions. Here we measure fluctuations in neuronal activity and blood volume associated with the same events across the mouse brain, and find that their relationship is consistent across brain regions but differs in two opposing brainwide neural populations. Functional Ultrasound Imaging (fUSI) revealed that whisking, a marker of arousal, is associated with brainwide fluctuations in blood volume. Simultaneous fUSI and Neuropixels recordings in cortex and hippocampus showed that neurons that increase vs. decrease activity with whisking have distinct hemodynamic response functions. Brainwide Neuropixels recordings revealed that these two opposing populations are present in the entire brain. When summed, their contributions predicted blood volume across brain regions better than predictions from bulk neural activity. The mouse brain thus contains two neural populations with opposite relation to brain state and distinct relationships to blood supply, which together account for brainwide fluctuations in blood volume.