Immune checkpoint therapy (ICPB) results in durable responses in individuals with some cancers, but not all patients respond to treatment. ICPB improves CD8+ cytotoxic T lymphocyte (CTL) function, but changes in tumor antigen-specific CTLs post-ICPB that correlate with successful responses have not been well characterized. Here, we studied murine tumor models with dichotomous responses to ICPB. We introduced a model tumor antigen (HA, hemagglutinin), tracked tumour (HA)-specific CTL frequencies and phenotype before and after ICPB in responding and non-responding animals. Tumor antigen-specific CTLs increased within tumor and draining lymph nodes after ICPB, and exhibited an effector memory-like phenotype, expressing IL-7R (CD127), KLRG1, T‑bet and granzyme B. Increased tumor antigen-specific CTLs corresponded to reduced TCR repertoire diversity within the tumor. Responding tumors exhibited higher infiltration of effector memory tumor antigen-specific CTLs, but lower frequencies of regulatory T cells compared to non-responders. Tumor antigen-specific CTLs persisted in responding animals and formed memory responses against tumor antigens. Our results suggest that increased effector memory tumor antigen-specific CTLs, in the presence of reduced immunosuppression within tumors is part of a successful ICPB response. Temporal and nuanced analysis of T cell subsets provides a potential new source of immune based biomarkers for response to ICPB.