Innate immunity is the first protection mechanism against invading pathogens and is critical for initiating adaptive immune responses to clear infections. As an obligate intracellular parasite, the immune protection against Toxoplasma gondii is governed by a robust secretion of interferon-gamma (IFNγ) by CD8+ T cells. However, the differentiation pathway that promotes IFNγ by the naïve CD8+ T cells is unclear. Our previous studies using naïve transnuclear CD8+ T cells (T57) to the endogenous T. gondii vacuolar resident antigen, TGD057, identified a novel pathway by which the microbial intracellular sensor NLR Family Pyrin Domain Containing 3 (NLRP3) is required for CD8+ T cells IFNγ responses in an inflammasome cascade-independent manner. Here we report a new requirement for eliciting this response through the activation of the cytosolic DNA sensor, STING, in T.gondii-infected cells. STING is a signal transducer for the presence of cyclic GMP-AMP (cGAMP) generated by the cytosolic DNA sensor cGAMP synthase (cGAS). However, we found only partial requirement for cGAS and IFNβ in this pathway, suggesting a novel mechanism by which STING promotes CD8+ T cell IFNγ differentiation. Our working model proposes that following T. gondii infection, NLRP3 and STING work independently of their conventional roles in the inflammasome and type I IFN response, which in turn promotes the IFNγ differentiation of naïve parasite-specific CD8+ T cells. Dissecting these less understood mechanisms for NLRP3 and STING could have important implications for vaccine design and clearance of protozoan pathogens.