Renal afferent arteriolar (AA) dilation is the major vascular alteration arising early during the course of type 1 diabetes (T1D); however, the underlying mechanism has not been established. Previously, we showed an enhanced tonic dilator impact of ATP-sensitive K⁺ channels (K _ATP) in afferent arterioles of rats with streptozotocin (STZ)-induced diabetes. We hypothesized that additional K⁺ channels contribute to AA dilation in STZ rats and that oxidative stress may play a role in altered K⁺ channel regulation of AA tone during T1D. We found that AA tone in normal kidneys was influenced by voltage-gated K⁺ channels, large-conductance Ca²⁺-activated K⁺ channels, and inward-rectifier K⁺ channels (K_IR channels). In contrast, neither tertiapin-Q-sensitive Kir1.1/3.x channels nor small-conductance Ca²⁺-activated K⁺ channels significantly contributed to setting basal tone in normal rat kidney. In kidneys from STZ rats, there emerged a tonic AA dilator impact of Kir1.1/3.x channels and an exaggerated dilator influence of Kir2.1 channels. Cultured preglomerular microvascular smooth muscle cells (PVSMCs) expressed Kir2.1, Kir1.1 and Kir6.1 at the mRNA level, but mRNA encoding Kir3.1, Kir3.4, Kir6.2 or Kir6.3 could not be detected. Culture of PVSMCs in high glucose media did not alter expression of any Kir family member. To address the role of oxidative stress in the mechanism of alter K⁺ channel regulation of AA tone in T1D, rats were treated chronically with the antioxidant, tempol. Tempol prevented the increased baseline AA diameter evident in STZ kidneys. Moreover, tempol prevented the exaggerated tonic impact of Kir2.1, Kir1.1 and Kir6.1 on afferent arterioles usually observed in kidneys from STZ rats. Protein expression of the K _IR channels in the preglomerular vasculature was not influenced by T1D or by tempol treatment of either sham or STZ rats. Tempol decreased T1D-induced renal oxidative stress, as measured by DHE staining and urinary H₂O ₂ excretion, although other indices of oxidant stress yielded conflicting results. We conclude that T1D decreases AA tone at least in part via effects on the K_IR family that likely involve post-translational mechanism(s) associated with oxidative stress.