Chronic alveolar hypoxia, whether due to residence at high altitude or lung disease, leads to a sustained increase in pulmonary vascular resistance and pulmonary hypertension. Strategies that augment endogenous nitric oxide (NO) production or activity, including L-arginine supplementation, attenuate the development of pulmonary hypertension. This action has previously been attributed to inhibition of vessel wall remodelling thus preventing structural narrowing of the vascular lumen. However, more recent evidence suggests that structural changes are not responsible for the elevated vascular resistance observed in chronic hypoxic pulmonary hypertension, calling into question the previous explanation for the action of L-arginine. We examined the effect of dietary L-arginine supplementation on pulmonary vasoconstriction, structurally-determined maximum vascular lumen diameter and vessel length during exposure of rats to hypoxia for two weeks. L-arginine attenuated the development of hypoxic pulmonary hypertension by preventing increased arteriolar resistance. It did not alter mean maximal vascular lumen diameter nor did it augment NO mediated vasodilatation in chronically hypoxic lungs. However, the total length of vessel within the gas exchange region of the hypoxic lungs was significantly increased following L-arginine supplementation. These findings suggest that dietary L-arginine ameliorated hypoxic pulmonary hypertension but not by an effect on the structurally determined lumen diameter of pulmonary blood vessels. L-arginine enhanced angiogenesis in the hypoxic pulmonary circulation which may attenuate hypoxic pulmonary hypertension by producing new parallel vascular pathways through the lung.