Influenza viruses circulate annually and cause significant morbidity and mortality during seasonal epidemics. CD8+ T cells provide broad protective immunity against influenza viruses. The quality of CD8+ T cell response against viral infections and its protective capacity can be influenced by Major histocompatibility complex (MHC) class I polymorphisms, binding affinity of T cell receptor (TCR)/peptide-MHC-I complex, functional avidity, and the nature of the TCRαβ repertoire. Here, we assessed at the single cell level, the TCRαβ repertoire and transcriptome of CD8+ T cells against an influenza-specific HLA-A*24:02-PB1498-505 (A24/PB1498) epitope, restricted by a human leukocyte antigen (HLA) allele frequently found in Indigenous Australians and associated with severe influenza disease during the pH1N1 outbreak. Using ex-vivo peptide-HLA tetramer-associated magnetic enrichment (TAME), single-cell multiplex-nested RT-PCR for paired TCRαβ repertoires, and TCRdist analysis of PBMCs from HLA-A*24:02 healthy donors, we assessed the quality of A24/PB1498+CD8+ T cells compared to the HLA-*02:01-M158 epitope, which is the most well-defined and immunodominant human influenza epitope restricted to the most common HLA-allele in Caucasians. We found that the TCRαβ repertoire of A24/PB1498+CD8+ T cells was biased in usage of TRBV9 (42.5%) with variable TRAV segment usage and highly diverse TCRαβ clonotypes. To further understand global qualitative differences between optimal A2/M158 and high-risk A24/PB1498 epitopes, we performed single-cell mRNA sequencing of peptide-HLA tetramer-specific CD8+ T cells ex vivo and showed that gene expression levels of cytotoxic molecules such as granzyme A, granzyme B and CCL5 were lower in A24/PB1498+CD8+ T cells than in A2/M158+CD8+ T cells. Overall, our findings provide new insights into the mortality-associated HLA-A*24:02 allomorph and suggest strategies to develop universal T cell-mediated vaccines and immunotherapies.