Individual growth is a fundamental life history trait, yet its macroevolutionary trajectories have rarely been investigated for entire animal assemblages. Here, we analyse the evolution of growth in a highly diverse vertebrate assemblage, coral reef fishes. We combined state-of-the-art extreme gradient boosted regression trees with phylogenetic comparative methods to detect the timing, number, location, and magnitude of shifts in the adaptive regime of somatic growth. We also explored the evolution of the allometric relationship between body size and growth. Our results show that the evolution of fast growth trajectories in reef fishes has been considerably more common than the evolution of slow growth trajectories. Many reef fish lineages shifted towards faster growth and smaller body size evolutionary optima in the Eocene (56-33.9 Ma), pointing to a major expansion of life history strategies in this Epoch. Of all lineages examined, the small-bodied, high-turnover cryptobenthic fishes shifted most towards extremely high growth optima, even after accounting for body size allometry. In concert, these results suggest that the high global temperatures of the Eocene and subsequent habitat reconfigurations might have been critical for the rise and retention of the highly productive, high-turnover fish faunas that characterise modern coral reef ecosystems.