During many chronic viral infections, the anti-viral T cell response becomes attenuated in a process that is partly host regulated. While elevated expression of the immunosuppressive cytokine IL-10 is involved in this process, the relevant cellular sources of IL-10, as well as the pathways responsible for IL-10 induction, remain unclear. In this study, we trace IL-10 production over the course of chronic lymphocytic choriomeningitis virus (LCMV) infection using an IL-10 reporter mouse line. We demonstrate that “exhausted” virus-specific T cells, particularly virus-specific Th1 cells, display elevated IL-10 expression during chronic LCMV infection and that ablation of IL-10 from the T cell compartment can partially restore T cell function and reduce viral loads. We find that Blimp-1 is required for IL-10 expression by Th1 cells and implicate antigen as the likely Blimp-1/IL-10 induction signal. Thus, effector T cells self-limit their responsiveness during persistent viral infection via an IL-10-dependent negative feedback loop.