T cell ageing has a pivotal role in rendering older individuals vulnerable to infections and cancer and in impairing the response to vaccination. Easy accessibility to peripheral human T cells as well as an expanding array of tools to examine T cell biology have provided opportunities to examine major ageing pathways and their consequences for T cell function. Here, we review emerging concepts of how the body attempts to maintain a functional T cell compartment with advancing age, focusing on three fundamental domains of the ageing process, namely self-renewal, control of cellular quiescence and cellular senescence. Understanding these critical elements in successful T cell ageing will allow the design of interventions to prevent or reverse ageing-related T cell failure.