Rationale: Inflammation is a prominent pathologic feature in pulmonary arterial hypertension as demonstrated by pulmonary vascular infiltration of inflammatory cells, including T and B lymphocytes. However, the contribution of the adaptive immune system is not well characterized in pulmonary hypertension caused by chronic hypoxia. CD4⁺ T cells are required for initiating and maintaining inflammation, suggesting these cells could play an important role in the pathogenesis of hypoxic pulmonary hypertension. Objectives: To test the hypothesis that CD4⁺ T cells, specifically the T helper 17 subset, contribute to chronic hypoxia-induced pulmonary hypertension. Methods: We compared indices of pulmonary hypertension resulting from chronic hypoxia (3 weeks) in wild-type mice and recombination-activating gene 1 knock-out mice (RAG1^-/-, lack mature T and B cells). Separate sets of mice were adoptively transferred with CD4⁺, CD8⁺, or T helper 17 cells prior to normoxic or chronic hypoxic exposure to evaluate the involvement of specific T cell subsets. Results: RAG1^-/- mice had diminished right ventricular systolic pressure and arterial remodeling compared to wild-type mice exposed to chronic hypoxia. Adoptive transfer of CD4⁺, but not CD8⁺ T cells, restored the hypertensive phenotype in RAG1^-/- mice. Interestingly, RAG1^-/- mice receiving T helper 17 cells displayed evidence of pulmonary hypertension independent of chronic hypoxia. Supporting our hypothesis, depletion of CD4⁺ cells or treatment with SR1001, an inhibitor of T helper 17 cell development, prevented increased pressure and remodeling responses to chronic hypoxia. Conclusions: T helper 17 cells play a key role in the development of chronic hypoxia-induced pulmonary hypertension.