We investigated the role of K⁺ channels in the regulation of baseline intracellular free Ca²⁺ concentration ([Ca²⁺]_i), -adrenoreceptor-mediated Ca²⁺ signaling, and capacitative Ca²⁺ entry in pulmonary artery smooth muscle cells (PASMCs). Inhibition of voltage-gated K⁺ channels with 4-aminopyridine (4-AP) increased the membrane potential and the resting [Ca²⁺]_i but attenuated the amplitude and frequency of the [Ca²⁺]_i oscillations induced by the -agonist phenylephrine (PE). Inhibition of Ca²⁺-activated K⁺ channels (with charybdotoxin) and inhibition (with glibenclamide) or activation of ATP-sensitive K⁺ channels (with lemakalim) had no effect on resting [Ca²⁺]_i or PE-induced [Ca²⁺]_i oscillations. Thapsigargin was used to deplete sarcoplasmic reticulum Ca²⁺ stores in the absence of extracellular Ca²⁺. Under these conditions, 4-AP attenuated the peak and sustained components of capacitative Ca²⁺ entry, which was observed when extracellular Ca²⁺ was restored. Capacitative Ca²⁺ entry was unaffected by charybdotoxin, glibenclamide, or lemakalim. In isolated pulmonary arterial rings, 4-AP increased resting tension and caused a leftward shift in the KCl dose-response curve. In contrast, 4-AP decreased PE-induced contraction, causing a rightward shift in the PE dose-response curve. These results indicate that voltage-gated K⁺ channel inhibition increases resting [Ca²⁺]_i and tone in PASMCs but attenuates the response to PE, likely via inhibition of capacitative Ca²⁺ entry.