The threat of influenza viruses to public health persists despite current vaccine strategies. Current vaccines induce predominantly antibody-mediated responses against the rapidly evolving influenza surface glycoproteins. Thus, when the circulating strains diverge from the vaccine strains, vaccine efficacy is lower. A more long-lasting strategy would be to target the conserved internal components of influenza viruses. CD8+ T cells are immune cells that recognise peptides presented on the surface of infected cells by Human Leukocyte Antigen class I molecules (HLA-I) – these peptides can include those from internal viral components. To understand which parts of influenza viruses are most useful for cross-strain protective immunity, we have developed a panel of lung epithelial cells expressing single common HLA-I variants for investigation of viral antigen presentation. We have established a workflow combining in vitro infection HLA-I peptide isolation and LC-MS/MS analysis, to allow characterization of influenza peptides presented by diverse HLA-I variants that are common in the human population. We have generated a map of HLA-I peptide presentation across several common HLA-I variants, revealing a rich proteome coverage of conserved regions of influenza virus. Proteome distribution analysis showed a wide breath of influenza peptides derived from highly conserved proteins, predominantly, matrix proteins, polymerase basic proteins and nucleoproteins. Influenza peptides from alternative reading frames were also detected. With in-depth exploration of conserved influenza targets and their immunogenicity profiles, our map of HLA-I influenza peptides will inform rational influenza vaccine design to offer long-lasting cross-strain protection mediated by CD8+ T cells.