Age-associated decreases in primary CD8 T cell responses occur, in part, due to direct effects on naïve CD8 T cells to reduce intrinsic functionality, but the precise nature of this intrinsic defect and its molecular basis remains to be defined. Ageing also causes accumulation of antigen-naïve but semi-differentiated “virtual memory” (T_VM) cells but their contribution to age-related functional decline is unclear. Here, we show that T_VM cells become non-proliferative in aged mice and humans, despite being highly proliferative in young individuals. Intriguingly, the proliferative function of conventionally defined naïve T cells (T_N cells) remained remarkably intact with age in both mice and humans. Adoptive transfer experiments in mice illustrated that the proliferative dysfunction acquired by T_VM cells was imposed by the aged environment but was not rescued by maintenance in a young environment. Further analysis of the mechanism underpinning the dysfunction demonstrated that aged T_VM cells exhibited a profile consistent with senescence, with increased Bcl-2 expression and phosphorylation of p38 and g-H2AX in steady state, along with increased Cdkn1a (p21) expression and defective cyclin D1 accumulation after TCR stimulation, marking the first description of senescence in an antigenically naïve T cell population. In summary, the age-related decline in primary CD8 T cell responses is associated with development of senescence in the semi-differentiated, formerly highly proliferative T_VM population, alongside a striking preservation of T_N cell function.