The hypothesized negative relationship between growth rate and lifespan has proved very difficult to test robustly because of potentially confounding variables, particularly nutrient availability and final size. Here we provide, to our knowledge, the first rigorous experimental test of this hypothesis, and find dramatic changes in lifespan in the predicted direction in response to both upward and downward manipulations of growth rates. We used brief (less than 4% of median lifespan) exposure to relatively cold or warm temperatures early in life to deflect juvenile three-spined sticklebacks Gasterosteus aculeatus from their normal growth trajectories; this induced catch-up or slowed-down growth when ambient temperatures were restored, and all groups attained the same average adult size. Catch-up growth led to a reduction in median lifespan of 14.5 per cent, while slowed-down growth extended lifespan by 30.6 per cent. These lifespan effects were independent of eventual size attained or reproductive investment in adult life. Photoperiod manipulations showed that the effects of compensatory growth on lifespan were also influenced by time available for growth prior to breeding, being more extreme when less time was available. These results demonstrate the growth-lifespan trade-off. While growing more slowly can increase longevity, the optimal resolution of the growth-lifespan trade-off is influenced by time constraints in a seasonal environment.