The role of epitope-specific regulatory CD4 T cells (Tregs) in modulating CD8 T cell-mediated immunopathology during acute viral infection has not been well defined. In the murine model of respiratory syncytial virus (RSV) infection, CD8 T cells play an important role in both viral clearance and immunopathology. We have previously characterized two RSV epitope-specific CD4 T cell responses with distinct phenotypic properties. One of them, the IA(b)M209-specific subset, constitutively expresses FoxP3 and modulates CD8 T cell function in vitro. Here, we show that the IA(b)M209-specific CD4 T cell response regulates CD8 T cell function in vivo and is associated with diminished RSV-induced illness without affecting viral clearance at the site of infection. Achieving the optimal balance of regulatory and effector T cell function is an important consideration for designing future vaccines.