Functional connectivity of the human brain changes through life. Here, we assemble task-free functional and structural magnetic resonance imaging data from 33,250 individuals at 32 weeks of postmenstrual age to 80 years from 132 global sites. We report critical inflection points in the nonlinear growth curves of the global mean and variance of the connectome, peaking in the late fourth and late third decades of life, respectively. After constructing a fine-grained, lifespan-wide suite of system-level brain atlases, we show distinct maturation timelines for functional segregation within different systems. Lifespan growth of regional connectivity is organized along a spatiotemporal cortical axis, transitioning from primary sensorimotor regions to higher-order association regions. These findings elucidate the lifespan evolution of the functional connectome and can serve as a normative reference for quantifying individual variation in development, aging and neuropsychiatric disorders.