Astrocytes can control basal synaptic strength and arteriole tone via their resting Ca activity. However, whether resting astrocyte Ca can adjust to a new steady-state level, with an impact on surrounding brain cells, remains unknown. Using two-photon Ca imaging in male rat acute brain slices of the somatosensory neocortex, we found that theta burst neural activity produced an unexpected long-lasting reduction in astrocyte free Ca in the soma and endfeet. The drop in intracellular Ca was attenuated by antagonists targeting multiple ionotropic and metabotropic glutamate receptors, and intracellular cascades involved Ca stores and nitric oxide. The reduction in astrocyte endfoot Ca was coincident with an increase in arteriole tone, and both the Ca drop and the tone change were prevented by an NMDA receptor antagonist. Astrocyte patch-clamp experiments verified that the glutamate receptors in question were located on astrocytes and that Ca changes within astrocytes were responsible for the long-lasting change in arteriole diameter caused by theta burst neural activity. In astrocytes from animals that lived in an enriched environment, we measured a relatively lower resting Ca level that occluded any further drop in Ca in response to theta burst activity. These data suggest that electrically evoked patterns of neural activity or natural experience can adjust steady-state resting astrocyte Ca and that the effect has an impact on basal arteriole diameter. The field of astrocyte-neuron and astrocyte-arteriole interactions is currently in a state of refinement. Experimental evidence suggests that direct manipulation of astrocyte-free Ca regulates synaptic signaling and local blood flow control; however, experiments fail to link synaptically evoked astrocyte Ca transients and immediate changes to various astrocyte-mediated processes. To clarify this discrepancy, we examined a different aspect of astrocyte Ca: the resting, steady-state free Ca of astrocytes, its modulation, and its potential role in the tonic regulation of surrounding brain cells. We found that or neural activity induced a long-lasting reduction in resting free astrocyte Ca and that this phenomenon changed arteriole tone.