Fruit have evolved a sophisticated tissue and cellular architecture to secure plant reproductive success. Postfertilization growth is perhaps the most dramatic event during fruit morphogenesis. Several studies have proposed that fertilized ovules and developing seeds initiate signaling cascades to coordinate and promote the growth of the accompanying fruit tissues. This dynamic process allows the fruit to conspicuously increase its size and acquire its final shape and means for seed dispersal. All these features are key for plant survival and crop yield. Despite its importance, we lack a high-resolution spatiotemporal map of how postfertilization fruit growth proceeds at the cellular level. In this study, we have combined live imaging, mutant backgrounds in which fertilization can be controlled, and computational modeling to monitor and predict post-fertilization fruit growth in Arabidopsis. We have uncovered that, unlike leaves, sepals, or roots, fruit do not exhibit a spatial separation of cell division and expansion domains; instead, there is a separation into temporal stages with fertilization as the trigger for transitioning to cell expansion, which drives postfertilization fruit growth. We quantified the coordination between fertilization and fruit growth by imaging no transmitting tract (ntt) mutants, in which fertilization fails in the bottom half of the fruit. By combining our experimental data with computational modeling, we delineated the mobility properties of the seed-derived signaling cascades promoting growth in the fruit. Our study provides the basis for generating a comprehensive understanding of the molecular and cellular mechanisms governing fruit growth and shape.