According to the current model of neurovascular coupling, brain blood flow is controlled regionally through phasic changes in the activity of neurons and astrocytes that signal to alter blood vessel diameter (1). This process is necessary to meet the energy demands of enhanced activity and is the basis of blood-oxygen-level-dependent (BOLD) functional MRI imaging. Previously absent from the neurovascular coupling framework was how basal brain blood flow is tonically regulated independent of phasic changes in activity, as well as how the brain controls the magnitude of blood delivery based the availability of oxygen. This is important because basal blood flow can influence the BOLD fMRI signal (2), becomes reduced in senescence (3), and is required to maintain a large fraction of total brain metabolic needs (4). We used two-photon fluorescence imaging combined with patch clamp electrophysiology in acute rat brain slices of sensory-motor cortex and hippocampus to demonstrate that astrocytes provide a steady-state vasodilation to arterioles via the constitutive release of prostaglandins. We show that the release of vasodilator is dependent on the resting Ca2+ activity in astrocyte endfeet and requires COX-1. Changing oxygen availability in the tissue controls the magnitude and direction of astrocyte diameter regulation, in which high oxygen promotes vasoconstriction pathways and low oxygen promotes vasodilation pathways when astrocytes are directly stimulated via Ca2+ uncaging (5). Finally, using two-photon imaging in fully awake mice in vivo, we demonstrate that acute COX-1 inhibition reduces resting arteriole diameter, but fails to affect functional hyperemia. Our findings delineate a form of brain blood flow control in which astrocytes play a vital role in controlling basal cerebral blood vessel tone in a manner that is sensitive to oxygen and uses cellular pathways that are independent of phasic, activity-dependent blood flow control.