Key points A locally generating, angiotensin II (ANG II) system is present in the rat carotid body (CB) and up‐regulation of this system occurs in certain pathophysiological situations, enhancing sympathetic activity. Here, we show that, similar to chemoreceptor type I cells, glial‐like type II cells also express functional AT 1 Rs, stimulation of which causes release of Ca 2+ from intracellular stores. ANG II–AT 1 R signalling in type II cells activates an inward current carried by pannexin‐1 (Panx‐1) channels which are known to act as conduits for release of ATP, a key CB excitatory neurotransmitter. Combined effects of ANG II and ATP, which also activates Panx‐1 currents via P2Y2 receptors, were synergistic; chelating intracellular Ca 2+ with BAPTA prevented Panx‐1 current activation. We propose that the excitatory function of ANG II in the CB involves dual actions at both type I and type II cells. Abstract A local angiotensin‐generating system is present in the carotid body (CB) and increased angiotensin II (ANG II) signalling contributes to enhanced CB excitation in chronic heart failure (CHF) and after chronic or intermittent hypoxia. ANG II actions have thus far been attributed solely to stimulation of AT 1 receptors (AT 1 Rs) on chemoreceptor type I cells. Here, we show that in dissociated rat CB cultures, ANG II also stimulates glial‐like type II cells, identified by P2Y2‐receptor‐induced intracellular Ca 2+ elevation (Δ[Ca 2+ ] i ). ANG II induced a dose‐dependent (EC 50 ∼8 n m ), robust Δ[Ca 2+ ] i in type II cells that was reversibly abolished by the AT 1 R blocker losartan (1 μ m ). The ANG II‐induced Δ[Ca 2+ ] i persisted in Ca 2+ ‐free medium but was sensitive to store depletion with cyclopiazonic acid (1 μ m ). Similar to P2Y2 receptor agonists, ANG II (20–1000 n m ) activated pannexin‐1 (Panx‐1) current that was reversibly abolished by carbenoxolone (5 μ m ). This current arose with a variable delay and was reversibly inhibited by losartan. Repeated application of ANG II often led to current run‐down, attributable to AT 1 R desensitization. When applied to the same cell the combined actions of ANG II and ATP on Panx‐1 current were synergistic. Current induced by either ligand was inhibited by BAPTA‐AM (1 μ m ), suggesting that intracellular Ca 2+ signalling contributed to Panx‐1 channel activation. Because open Panx‐1 channels release ATP, a key CB excitatory neurotransmitter, it is plausible that paracrine stimulation of type II cells by ANG II contributes to enhanced CB excitability, especially in pathophysiological conditions such as CHF and sleep apnoea.