The capillary/arteriole complex is the key operational unit regulating local perfusion to meet metabolic demand. However, much remains to be learned about how this multi cellular unit is functionally organized. To help address this challenge, we characterized the electrotonic architecture of the retinal microvasculature, which is particularly well adapted for the decentralized control of blood flow. In this study, we quantified the transmission of voltage between pairs of perforated-patch pipettes sealed onto abluminal cells located on microvascular complexes freshly isolated from the adult rat retina. These complexes consisted of capillaries,as well as tertiary and secondary arterioles. Dual recording experiments revealed that voltage spreading axially through a capillary, tertiary arteriole or secondary arteriole is transmitted very efficiently with a decay rate of only ∼5% per 100 μm. However, the retinal microvasculature is not simply a well-coupled syncytium since we detected significant voltage dissipation with radial abluminal cell-to-endothelium transmission and also at branch points between a capillary and its tertiary arteriole and between tertiary and secondary arterioles. Consistent with capillaries being particularly well-suited for the task of transmitting voltages induced by vasoactive signals, radial transmission is most efficient in this portion of the retinal microvasculature. Dual recordings also revealed that angiotensin II potently inhibits axial transmission. As a functional consequence, the geographical extent of the microvasculature's response to voltage-changing inputs is markedly restricted in the presence of angiotensin. In addition, this effect of angiotensin established that the electrotonic architecture of the retinal microvasculature is not static, but rather, is dynamically modulated by vasoactive signals.