Pregnant women are at increased risk of severe respiratory virus infections like influenza and COVID-19, and re-activation of chronic viruses such as cytomegalovirus (CMV). While it is well-established that CD8+ T cells have an important role in the control and clearance of viral infections, less is known on how pregnancy impacts the establishment, phenotype and function of epitope-specific CD8+ T cells across different viruses. To address this, we performed single-cell RNAseq, CITEseq, and TCRseq on epitope-specific CD8+ T cells using peptide-HLA-I-DNA-oligo dextramers specific for influenza A virus (IAV), SARS-CoV-2, respiratory syncytial virus (RSV), Epstein-Barr virus (EBV), and CMV in pregnant and non-pregnant peripheral blood, and pregnancy-matched decidual tissue from HLA-A*02:01+ individuals. Analysis of CD8+ T cells directed towards acute respiratory viruses (IAV, SARS-CoV-2, RSV) showed lower expression of RNA encoding cytotoxic granules and inhibitory receptors during pregnancy. Meanwhile, in chronic virus-specific (EBV, CMV) CD8+ T cells, pregnant women had increased cytotoxic granule RNA expression and altered surface expression of chemokine receptors CX3CR1 and CCR5, indicating a more “effector-like” phenotype in pregnancy. Within the immunodominant epitopes A2/M158 (IAV), A2/pp65465 (CMV), and A2/BMLF1280 (EBV) we identified common T cell receptor (TCR) gene usages in pregnant and non-pregnant blood and decidua. We provide the first report of decidual IAV-specific CD8+ T cells, which had similar TCR gene usage as the respective donor-matched peripheral blood. Additional analyses into acute vs chronic virus-specific CD8+ T cells identified key gene signatures associated with each of the 5 virus specificities. Further experiments on acute and chronic virus epitope-specific CD8+ T cells from pregnant and non-pregnant women will help us better understand the mechanisms underlying the altered phenotype in pregnancy. Taken together, these data suggest that pregnancy alters CD8+ T cell immunity in a virus-specific manner and provide novel insights that reveal potential targets for immunotherapies during pregnancy.