The inability to quantify cerebral blood flow and changes in macrocirculation cross-sectional area in all brain regions impedes robust insight into hypoxic cerebral blood flow control. We applied four-dimensional flow magnetic resonance imaging to quantify cerebral blood flow (ml • min⁻¹) and cross-sectional area (mm²) simultaneously in 11 arteries. In healthy adults, blood pressure, O₂ Saturation (SpO₂), and end-tidal CO₂ were measured at baseline and steady-state hypoxia (FiO₂ = 0.11). We investigated left and right: internal carotid, vertebral, middle, anterior, posterior cerebral arteries, and basilar artery. Hypoxia (SpO₂ = 80±2%) increased total cerebral blood flow from 621±38 to 742±50 ml • min⁻¹ (p < 0.05). Hypoxia increased cerebral blood flow, except in the right posterior cerebral arteries. Hypoxia increased cross-sectional area in the anterior arteries (left and right internal carotid arteries, left and right middle, p < 0.05; left and right anterior p = 0.08) but only the right vertebral artery of the posterior circulation. Nonetheless, relative cerebral blood flow distribution and vascular reactivity (Δ%cerebral blood flow • ΔSpO₂⁻¹) were not different between arteries. Collectively, moderate hypoxia: (1) increased cerebral blood flow, but relative distribution remains similar to normoxia, (2) evokes similar vascular reactivity between 11 arteries, and (3) increased cross-sectional area primarily in the anterior arteries. This study provides the first wide-ranging, quantitative, functional and structural data regarding intracranial arteries during hypoxia in humans, highlighting cerebral blood flow regulation of microcirculation and macrocirculation differs between anterior and posterior circulation.