The brain has evolved mechanisms to dynamically modify blood flow, enabling the timely delivery of energy substrates in response to highly fluctuating local metabolic demands. Several such neurovascular coupling mechanisms have been identified, but the vascular signal transduction and transmission mechanisms that enable dilation of penetrating arterioles remote from sites of increased neuronal activity are unclear. Given the exponential relationship between vessel diameter and blood flow, tight control of arteriole smooth muscle membrane potential and diameter is a crucial aspect of neurovascular coupling. Recent evidence suggests that that capillaries play a major role in sensing neural activity and transmitting signals to modify the diameter of upstream vessels. Thin-strand pericyte processes cover around 90% of the capillary bed but their contributions to blood flow control are not understood. We show that thin-strand pericytes play a central role in neurovascular coupling by sensing neural activity and generating and relaying electrical signals to arteriolar smooth muscle. We identify a K_ATP channel-dependent neurovascular signaling pathway that is explained by the recruitment of capillary pericytes, and deploy vascular optogenetics to show that currents generated in individual thin-strand pericytes are sent over long distances to upstream arterioles in vivo to cause dilations. Genetic disruption of vascular K_ATP channels reduces the arteriole diameter response to neural activity and laser ablation of thin-strand pericytes eliminates the K_ATP-dependent component of neurovascular coupling. Our work indicates that thin-strand pericytes actively sense neural activity and transform this into K_ATP channel-dependent electrometabolic signals that inform upstream arteriolar smooth muscle of local energy needs, promoting spatiotemporally precise energy distribution.