This study examined whether elevated intravascular pressure stimulates asynchronous Ca²⁺ waves in cerebral arterial smooth muscle cells and if their generation contributes to myogenic tone development. The endothelium was removed from rat cerebral arteries, which were then mounted in an arteriograph, pressurized (20–100 mmHg) and examined under a variety of experimental conditions. Diameter and membrane potential (V_M) were monitored using conventional techniques; Ca²⁺ wave generation and myosin light chain (MLC₂₀)/MYPT1 (myosin phosphatase targeting subunit) phosphorylation were assessed by confocal microscopy and Western blot analysis, respectively. Elevating intravascular pressure increased the proportion of smooth muscle cells firing asynchronous Ca²⁺ waves as well as event frequency. Ca²⁺ wave augmentation occurred primarily at lower intravascular pressures (<60 mmHg) and ryanodine, a plant alkaloid that depletes the sarcoplasmic reticulum (SR) of Ca²⁺, eliminated these events. Ca²⁺ wave generation was voltage insensitive as Ca²⁺ channel blockade and perturbations in extracellular [K⁺] had little effect on measured parameters. Ryanodine‐induced inhibition of Ca²⁺ waves attenuated myogenic tone and MLC₂₀ phosphorylation without altering arterial V_M. Thapsigargin, an SR Ca²⁺‐ATPase inhibitor also attenuated Ca²⁺ waves, pressure‐induced constriction and MLC₂₀ phosphorylation. The SR‐driven component of the myogenic response was proportionally greater at lower intravascular pressures and subsequent MYPT1 phosphorylation measures revealed that SR Ca²⁺ waves facilitated pressure‐induced MLC₂₀ phosphorylation through mechanisms that include myosin light chain phosphatase inhibition. Cumulatively, our findings show that mechanical stimuli augment Ca²⁺ wave generation in arterial smooth muscle and that these transient events facilitate tone development particularly at lower intravascular pressures by providing a proportion of the Ca²⁺ required to directly control MLC₂₀ phosphorylation.