Stomatal response to environmental conditions forms the backbone of all ecosystem and carbon cycle models, but is largely based on empirical relationships. Evolutionary theories of stomatal behavior can guard against out-of-sample errors in the empirical models. Longstanding theory holds that plants optimize carbon gain per unit water lost – i.e. constant marginal water use efficiency – but a new evolutionary theory proposes that stomata maximize carbon gain minus costs of hydraulic damage. The two theories predict different responses to drought, and thus divergent out-of-sample predictions for future climates. Using data from 34 species that span global forest biomes, we find that this carbon-maximization optimization is supported at timescales from days to years, revealing that marginal water use efficiency is not the quantity that governs the evolution of stomatal regulation of plant water loss.