T cells play important roles in protection during dengue virus (DENV) infection and in the immunopathogenesis of dengue fever. Using mass cytometry and a highly-multiplexed peptide-HLA tetramer staining strategy, we probed T cells from dengue patients for a total of 430 dengue and control candidate epitopes presented on HLA A*1101, A*2402, and B*5801, together with key markers of activation, trafficking, and differentiation. We found that expression of PD-1, ICOS, CD39, CD69, and GPR56 on dengue-specific T cells varied significantly depending on HLA type. We also phenotypically profiled diverse T cell subsets and NK cells. Acute dengue infection resulted in broad activation and proliferation of these cells. During the acute stage, denguespecific CD8 + T cells expressed a unique profile of activation and trafficking receptors that distinguished them from non-dengue specific T cells. During convalescence dengue-specific T cells differentiated into two major cell fates, CD57 + CD127terminally differentiated senescent memory cells and CD127 + CD57proliferation-capable memory cells. The long-term maintenance of dengue-specific T cells with these phenotypes was evaluated in a second cohort of dengue patients and these subsets were found at elevated frequencies up to one year after infection. These analyses aid our understanding of the generation of T cell memory in dengue infection or vaccination.