Tuberculosis remains a leading cause of death globally, and approximately 5-10% of those infected develop pulmonary disease, often after initially controlling infection. Why immunity fails is unknown. CD4 T cells are crucial for immunity against Mtb, yet little is known about how Mtb infection might modulate CD4 T cell function, particularly late during infection. We hypothesize that failure of CD4 T cell function permits bacterial recrudescence and the development of active disease. Here, we develop a minimalistic adoptive transfer model to study antigen-specific T cells in the lungs of Mtb-infected mice. Late during infection, a decrease in T cell polyfunctionality and production of IL-2, TNF, and IFNγ is accompanied by the accumulation of PD-1 and TIM-3 expressing T cells. Transcriptional profiling identifies signatures of senescence and exhaustion in these cells. In C57Bl/6 mice, a similar co-inhibitory receptor expression and loss of function is observed on antigen-specific CD4s. Single-cell sequencing reveals that most expanded parenchymal T cells are hypofunctional, even early post-infection. However, no evidence of exhaustion or senescence was found. As TCR affinity and signaling strength affects T cell differentiation, we next examined whether TCR affinity impacts T cell function. Higher affinity CD4 T cells differentiate into polyfunctional Th1 cells while lower affinity clones skew towards a Th17 phenotype. The distinct clusters formed by high and low affinity clones on a UMAP projection show how TCR signaling strength affects T cell differentiation during chronic infection. These data provide insight into mechanisms modulating CD4 T cell dysfunction during chronic infection. Further study into these mechanisms will inform therapeutic options.