In the microcirculation, longitudinal conduction of vasomotor responses provides an essential means of coordinating flow distribution among vessels in a complex network. Spread of current along the vessel axis can display a regenerative component, which leads to propagation of vasomotor signals over many millimeters; the ionic basis for the regenerative response is unknown. We examined the responses to 10s of focal electrical stimulation (30Hz, 2ms, 30V) of mouse cremasteric arterioles to test the hypothesis that voltage-dependent Na⁺ (Na_v) and Ca⁺⁺ channels can be activated in long-distance signaling in micro-vessels. Electrical stimulation evoked a vasoconstriction at the site of stimulation and a spreading, non-decremental conducted dilation. Endothelial damage (air bubble) blocked the conduction of the vasodilation, indicating an involvement of the endothelium. The Na_v blocker, bupivicaine also blocked conduction and tetrodotoxin attenuated it. The Na_v activator, veratridine, induced an endothelium-dependent dilation. The Na_v isoforms Na_v1.2, Na_v1.6 and Na_v1.9 were detected in the endothelial cells of cremasteric arterioles by immunocytochemistry. These findings are consistent with the involvement of Na_v channels in the conducted response. BAPTA buffering of endothelial cell Ca⁺⁺ delayed and reduced the conducted dilation, which was almost eliminated by Ni⁺⁺, amiloride, or deletion of _1H T-type Ca++ channels (Ca_v3.2). Blockade of endothelial nitric oxide synthase (eNOS) or Ca⁺⁺-activated K⁺ channels (K_Ca) also inhibited the conducted vasodilation. Our findings indicate that an electrically induced signal can propagate along the vessel axis via the endothelium and can induce sequential activation of Na_v and Ca_v3.2. The resultant Ca⁺⁺ influx activates both eNOS and K_Ca, triggering vasodilation.