The regulation of brain blood flow is critical for maintaining tissue health. Ultra-slow and rhythmic fluctuations in blood vessel diameter – termed vasomotion – is important for ensuring adequate tissue perfusion and oxygen delivery under resting-state conditions. Yet, the mechanisms regulating very low frequency oscillations in arteriole tone/cerebral blood flow remain poorly understood. Astrocytes possess numerous Ca2+-dependent vasoactive signaling pathways and are in close contact with both the microvasculature and the neurons that entrain vasomotion, making them prime candidates for the ongoing modulation of resting cerebral perfusion. I tested the hypothesis that bidirectional communication between endfeet and arterioles controls multiple arteriole tone states ex vivo and ultra-slow rhythmic arteriole oscillations in vivo. Using simultaneous two-photon microscopy and patch clamp electrophysiology, I discovered in acute cortical brain slices that clamping astrocyte Ca2+ at a low physiological level (25 nM) produced vasoconstriction dependent on COX-1 activity, as demonstrated through both pharmacological COX-1 blockade and transgenic astrocyte-specific COX-1 knockdown. Using vascular chemogenetics, I found that ex vivo induction of vasoconstriction elicits an increase in astrocyte Ca2+ via TRPV4 activation. In turn, TRPV4-mediated Ca2+ elevation in astrocyte endfeet recruits feedback vasodilation through COX-1 activity to limit the extent of vasoconstriction. From in vivo recordings, I found that astroglial COX-1 knockdown increased power across both across ultra-slow (0.01-0.05Hz) and ‘vasomotion’ (0.05-0.3Hz) frequency ranges, indicating that astrocyte COX-1 constrains spontaneous fluctuations in arteriole diameter. In contrast, clamping astrocyte Ca2+ in vivo via a astrocyte-specific Ca2+ extrusion pump reduced power across the vasomotion frequency band, suggesting an important role for astrocyte in facilitating diameter oscillations. Next, I tested how a direct and sustained exogenous elevation in astrocyte Ca2+ impacts arteriole tone and found that clamping Ca2+ at a moderately elevated level (250nM) above an approximate resting Ca2+ concentration (100 nM) elicited long-lasting vasodilation dependent on COX-1 activity, whereas a high Ca2+ concentration (750nM) produced vasoconstriction that was dependent on 20-HETE signaling. These data demonstrate that astrocytes participate in the ongoing regulation of cerebral blood flow by both sensing and inducing arteriole tone changes. These novel mechanisms of bidirectional communication between astrocytes and microvasculature suggest a new means whereby cerebral perfusion may be matched with the metabolic needs of the tissue, which is critical for brain health and function.