CD8+ T cells form a crucial arm of the adaptive immune system and act as sentinels against infection and cancer. The role of autophagy, a major lysosomal degradation pathway, in T cell biology is currently limited. Here, we show that autophagy is required for naïve CD8+ T cell homeostasis. When the essential autophagy gene Atg7 is deleted in the T cell lineage (T-Atg7^-/- mice), mice develop lymphopaenia leading to increased CD8+ T cell homeostatic proliferation. When CD8+ T cells encounter antigen, they undergo an initial expansion before contracting, leaving behind a population of long-lived memory cells that provide long-lasting immunity. How CD8+ T cells utilise autophagy when responding to infection is currently unknown. We demonstrate that autophagy is dispensable for CD8+ T cell expansion, but loss of Atg7 results in the failure to establish CD8+ T cell memory to influenza and MCMV infection. Interestingly, CD8+ T cell memory becomes defective in old age, although the cellular mechanism for this is largely unknown. Here, aged mice were shown to exhibit defective CD8+ T cell expansion and memory formation to immunisation. Autophagy levels were diminished in antigen-specific CD8+ T cells from aged mice and the CD8+ T cell response of old mice to vaccination could be rejuvenated in an autophagy-dependent manner using the compound spermidine. These results suggest that targeting of the autophagy pathway might be beneficial as a route to effective T cell modulation and enhanced immunity to infection and vaccination.