The brain capillary network represents an active signaling interface that dynamically regulates cerebral blood flow (CBF). Capillary endothelial cells (cECs) and pericytes form the functional core of this network, integrating neuronal and metabolic cues through specialized ion channel signaling pathways that govern membrane potential (V_M) and electrical communication. However, the molecular mechanisms underlying ion channel-mediated signaling within the capillary network remain incompletely understood. Using complementary electrophysiological, imaging, and in vivo approaches — including transgenic mouse models with cell-specific manipulation of ion channel function — we characterized the ion channel repertoire of brain cECs and pericytes. Our studies demonstrate that K_ATP channels are functionally expressed in both cECs and pericytes, where they mediate adenosine-induced hyperpolarization and increases in CBF through an A_2A receptor-Gα_s/cAMP/PKA signaling pathway, identifying capillary K_ATP channels as key regulators of CBF. We further show that pericytes express a diverse repertoire of K⁺ channels, including Kir2, K_V1 and BK_Ca channels, providing complementary mechanisms for setting pericyte V_M, modulating capillary hemodynamics, and regulating CBF. Finally, we identified functional hyperpolarization-activated, cyclic nucleotide-gated (HCN) channels in brain endothelial cells, revealing a previously unrecognized cAMP-sensitive conductance. Rather than acting as signal-generating pacemaker channels, as in cardiomyocytes and neurons, endothelial HCN channels may function as terminators of propagating hyperpolarizing signals— a conceptual departure from their canonical role in excitable tissues.