We applied multimodal microscopic imaging of intravascular partial pressure of O2 (PO2) and blood flow complemented by numerical modeling to reveal the properties of the cortical microvascular oxygenation that allow uninterrupted oxygen delivery to all tissue regions in a very dynamic and energetically demanding brain. Our measurements show that at the baseline level of neuronal activity small arterioles are responsible for a significant oxygen extraction, while the most of the remaining oxygen release is taking place at the level of the first few capillary branches after precapillary arterioles. The majority of capillaries (i.e. high branching order capillaries) release little O2 at rest and our measurements and modeling show that they act as a dynamic O2 reserve that is recruited on demand to ensure adequate tissue oxygenation during increased neuronal activity or decrease in blood flow. These findings have potential to overturn our textbook knowledge of the capillary oxygen delivery, impact our understanding of progression of diseases that affect cerebral microcirculation, and help improving the quantitative interpretation of brain imaging modalities.