L-type voltage-dependent calcium (Ca²⁺) channels, ryanodine-sensitive Ca²⁺ release (RyR) channels, and large-conductance Ca²⁺-activated potassium (K_Ca) channels comprise a functional unit that regulates smooth muscle contractility. Here, we investigated whether genetic ablation of caveolin-1 (cav-1), a caveolae protein, alters Ca²⁺ spark to K_Ca channel coupling and Ca²⁺ spark regulation by voltage-dependent Ca²⁺ channels in murine cerebral artery smooth muscle cells. Caveolae were abundant in the sarcolemma of control (cav-1^+/+) cells, but not observed in cav-1 deficient (cav-1^-/-) cells. Ca²⁺ spark and transient K_Ca current frequency were ~2-fold higher in cav-1^-/- than in cav-1^+/+ cells. Although voltage-dependent Ca²⁺ current density was similar in cav-1^+/+ and cav-1^-/- cells, diltiazem and Cd²⁺, voltage-dependent Ca²⁺ channel blockers, reduced transient K_Ca current frequency to ~55 % of control in cav-1^+/+ cells, but did not alter transient K_Ca current frequency in cav-1^-/- cells. Furthermore, although K_Ca channel density was elevated in cav-1^-/- cells, transient K_Ca current amplitude was similar to that in cav-1^+/+ cells. Higher Ca²⁺ spark frequency in cav-1^-/- cells was not due to elevated intracellular Ca²⁺ concentration, sarcoplasmic reticulum Ca²⁺ load, or NOS activity. Similarly, Ca²⁺ spark amplitude and spread, the percentage of Ca²⁺ sparks that activated a transient K_Ca current, the amplitude relationship between sparks and transient K_Ca currents, and K_Ca channel conductance and apparent Ca²⁺-sensitivity were similar in cav-1^+/+ and cav-1^-/- cells. In summary, cav-1 ablation elevates Ca²⁺ spark and transient K_Ca current frequency, attenuates the coupling relationship between voltage-dependent Ca²⁺ channels and RyR channels that generate Ca²⁺ sparks, and elevates K_Ca channel density, but does not alter transient K_Ca current activation by Ca²⁺ sparks. These findings indicate that cav-1 is required for physiological Ca²⁺ spark and transient K_Ca current regulation in cerebral artery smooth muscle cells.