Gammaherpesvirus infection in AIDS patients is associated with severe disease. Progressive loss of CD4 T cells results in an erosion of immune surveillance, which may lead to gammaherpesvirus associated tumors. Studies by our group and others have used murine γHV-68 infection in combination with CD4 depletion to model this breakdown in immune surveillance. Mice initially control the infection, but virus reactivates after 6 weeks, indicating a lack of long-term immune surveillance. We previously showed mice had elevated IL-10 and therapeutic IL-10R blockade reduced reactivation of the virus, implicating IL-10 as a key factor suppressing immune surveillance. We identified a population of IL-10 producing CD8 T cells only in the infected mice lacking CD4 T cells but not in intact mice. Here we characterize IL-10+ CD8 T cells and elucidate how they arise in both the acute and chronic phase of the infection. In the acute phase of the infection less IL-10 producing CD8s arose in the absence of CD4 help or CD40-CD40L signaling, while in the chronic phase IL-10+ CD8s only arose in the absence of CD4 help. IL-10 producing CD8s in the chronic phase showed an anergic phenotype in terms of proliferation in vitro. In addition, they suppressed the proliferation of effector CD8 T cell in vitro. Dissection of the mechanisms involved in the generation and the function of these suppressive IL-10 producing CD8 T cells may expose new targets for therapeutic intervention for AIDS patients.