T cell activation and function depend on Ca²⁺signals mediated by store-operated Ca²⁺entry (SOCE) through Ca²⁺release–activated Ca²⁺(CRAC) channels formed by ORAI1 proteins. We here investigated how SOCE controls T cell function in pulmonary inflammation during a T helper 1 (T_H1) cell–mediated response to influenza A virus (IAV) infection and T_H2 cell–mediated allergic airway inflammation. T cell–specific deletion ofOrai1did not exacerbate pulmonary inflammation and viral burdens following IAV infection but protected mice from house dust mite–induced allergic airway inflammation. ORAI1 controlled the expression of genes including p53 and E2F transcription factors that regulate the cell cycle in T_H2 cells in response to allergen stimulation and the expression of transcription factors and cytokines that regulate T_H2 cell function. Systemic application of a CRAC channel blocker suppressed allergic airway inflammation without compromising immunity to IAV infection, suggesting that inhibition of SOCE is a potential treatment for allergic airway disease.