Production of armed effector CD8+ T cells during persistent infection requires a stable pool of stem-like cells that can give rise to short-lived effector T cells via a proliferative intermediate population. In chronic infection models marked by T cell exhaustion, this process can be transiently induced by check-point blockade, but it occurs spontaneously and continuously in the spleens of mice chronically infected with the protozoan intracellular parasite, Toxoplasma gondii, providing a unique opportunity to examine the steps in the differentiation process. Using this model, we observed distinct locations and gene expression patterns for stem-like memory cells, proliferative intermediate cells, and terminally differentiated effector cells, implying a link between differentiation and discrete anatomical niches in the spleen. Loss of the chemokine receptor CXCR3 on parasite-specific T cells did not impair their white pulp to red pulp migration but reduced their interactions with CXCR3 ligand-producing type 2 conventional DCs in the bridging channels and impaired their transition from memory to intermediate states, leading to a build up of memory T cells localized to the red pulp. These results demonstrate a critical role for CXCR3 during chronic infection by increasing T cell exposure to differentiation-inducing signals during red pulp migration, providing a dynamic and flexible mechanism for modulating effector differentiation in response to environmental signals. While mice chronically infected with T. gondii are able to effectively establish long-term control of the pathogen, they do not establish sterilizing immunity. Although the parasite is primarily restricted to the brain during the chronic phase of infection, CD8+ T cells in the periphery experience continuous antigenic stimulation, resulting in ongoing proliferation and effector differentiation. We investigated the role of IFNγ in regulating CD8+ T cell fate during chronic T. gondii infection. We observed that neutralization of IFNγ during chronic infection led to dramatic changes in CD8+ T cell fate, promoting robust proliferation at the expense of terminal effector differentiation. These changes in CD8+ T cell fate were dependent on CXCR3 and linked to increases in antigen presentation in the spleen, which occurred in the absence of widespread parasite reactivation. Finally, IFNγ neutralization resulted in the emergence of clusters of CD11c+ cells in the red pulp of the spleen that were robust producers of CXCR3 ligands and supported a proliferation rich-environment. These results highlight an ongoing role for IFNγ in mediating the clearance of T. gondii antigens during chronic infection and contribute to our understanding of the factors regulating CD8+ T cell fate.