The membrane potential of vascular smooth muscle cells is determined, in large part, by K⁺ channels. In the companion paper, we demonstrate that superior mesenteric arteries from rats made hypertensive with L-NNA (N^w-nitro-L-arginine) are depolarized compared to normotensive rats. Further, L-NNA hypertension is associated with reduced molecular expression of two K⁺ channel proteins: KV1.5 (voltage-sensitive delayed rectifier) and BK_Ca subunit (Ca²⁺/voltage-sensitive). In the present study, we used patch clamp techniques to test the hypothesis that L-NNA-induced hypertension reduces the functional expression of K⁺ channels in smooth muscle cells. In whole-cell experiments using a Ca²⁺-free pipette solution, current at 0 mV, largely due to delayed rectifier K⁺ channels, was reduced ~60% in smooth muscle cells from hypertensive rats (2.7 ± 0.4 vs. 1.1 ± 0.2 pA/pF). Current at +100 mV with 300 nM free Ca²⁺, largely due to BKCa channels, was reduced ~40% in smooth muscle cells from hypertensive rats (181 ± 24 vs. 101 ± 28 pA/pF). Current blocked by 3 mM 4 aminopyridine, an inhibitor of many KV channel types (including KV1.5), was reduced ~50% in smooth muscle cells from hypertensive rats (1.0 ± 0.4 vs. 0.5 ± 0.2 pA/pF). Current blocked by 1 mM tetraethylammonium, an inhibitor of BK_Ca channels, was reduced ~40% in myocytes from hypertensive rats (86 ± 14 vs. 53 ± 19 pA/pF). Differences in BKCa current magnitude are not attributable to changes in single channel conductance or Ca²⁺/voltage-sensitivity. The data support the hypothesis that L-NNA-induced hypertension reduces macroscopic K⁺ current in vascular smooth muscle. Reduced molecular and functional expression of K⁺ channels may partly explain the depolarization and augmented contractile sensitivity of smooth muscle from L-NNA-treated rats.