The cerebral arteries of hypertensive rats are depolarized and highly myogenic, suggesting a loss of K⁺ channels in the vascular smooth muscle cells (VSMCs). The present study evaluated whether the dilator function of the prominent Shaker-type, voltage-gated K⁺ (K_v1) channels is attenuated in middle cerebral arteries from two rat models of hypertension. Block of K_v1 channels by correolide (1 µmol/L) or psora-4 (100 nmol/L) reduced the resting diameter of pressurized (80 mm Hg) cerebral arteries from normotensive rats by an average of 28 ± 3% or 26 ± 3%, respectively. In contrast, arteries from spontaneously hypertensive rats (SHR) and aortic-banded (Ao-B) rats with chronic hypertension showed enhanced Ca²⁺-dependent tone and failed to significantly constrict to correolide or psora-4, implying a loss of K_v1 channel -mediated vasodilation. Patch-clamp studies in the VSMCs of SHR confirmed that the peak K⁺ current density attributed to K_v1 channels averaged only 5.47 ± 1.03 pA/pF compared to 9.58 ± 0.82 pA/pF in VSMCs of control Wistar-Kyoto rats. Subsequently, Western blots revealed a 49 ± 7% to 66 ± 7% loss of the pore-forming 1.2 and 1.5 subunits that compose K_v1 channels in cerebral arteries of SHR and Ao-B rats compared to control animals. In each case, the deficiency of K_v1 channels was associated with reduced mRNA levels encoding either or both subunits. Collectively, these findings demonstrate that a deficit of 1.2 and 1.5 subunits results in a reduced contribution of K_v1 channels to the resting diameters of cerebral arteries from two rat models of hypertension that originate from different etiologies.