This review considers the relationship between the lifespan of an individual plant and the longevity of its component cells, tissues and organs. It begins by defining the terms senescence, growth, development, turnover, ageing, death and program. Genetic and epigenetic mechanisms regulating phase change from juvenility to maturity influence directly the capacity for responding to senescence signals and factors determining reproduction-related patterns of deteriorative ageing and death. Senescence is responsive to communication between sources and sinks in which sugar signalling and hormonal regulation play central roles. Monocarpy and polycarpy represent contrasting outcomes of the balance between the determinacy of apical meristems and source–sink cross-talk. Even extremely long-lived perennials sustain a high degree of meristem integrity. Factors associated with deteriorative ageing in animals, such as somatic mutation, telomere attrition and the costs of repair and maintenance, do not seem to be particularly significant for plant lifespan, but autophagy-related regulatory networks integrated with nutrient signalling may have a part to play. Size is an important influence on physiological function and fitness of old trees. Self-control of modular structure allows trees to sustain viability over prolonged lifespans. Different turnover patterns of structural modules can account for the range of plant life histories and longevities.