Male reproductive success is an extremely variable fitness component. Understanding the maintenance of this variation is a key challenge in evolutionary biology. An often neglected source of variation in male reproductive success is determined by age-dependent patterns of decline in sperm fitness. Two pathways mediate sperm senescence: pre-meiotic senescence of somatic and germ cells of the ageing male, and post-meiotic ageing of the spermatozoon. Recently, theoretical and empirical studies have highlighted wide-ranging implications of both pathways. We clarify different mechanisms of sperm senescence, outlining their distinct evolutionary implications for the male, the female and the zygote, and their influence on fundamental evolutionary processes, including the evolution of anisogamy, sexual conflict, sexual selection, and applied issues such as assisted conception.