C4 photosynthesis is a complex set of leaf anatomical and biochemical adaptations that have evolved more than 60 times to boost carbon uptake compared with the ancestral C3 photosynthetic type1,​2,​3. Although C4 photosynthesis has the potential to drive faster growth rates4,5, experiments directly comparing C3 and C4 plants have not shown consistent effects1,6,7. This is problematic because differential growth is a crucial element of ecological theory8,9 explaining C4 savannah responses to global change10,11, and research to increase C3 crop productivity by introducing C4 photosynthesis12. Here, we resolve this long-standing issue by comparing growth across 382 grass species, accounting for ecological diversity and evolutionary history. C4 photosynthesis causes a 19–88% daily growth enhancement. Unexpectedly, during the critical seedling establishment stage, this enhancement is driven largely by a high ratio of leaf area to mass, rather than fast growth per unit leaf area. C4 leaves have less dense tissues, allowing more leaves to be produced for the same carbon cost. Consequently, C4 plants invest more in roots than C3 species. Our data demonstrate a general suite of functional trait divergences between C3 and C4 species, which simultaneously drive faster growth and greater investment in water and nutrient acquisition, with important ecological and agronomic implications.