Summary Photosynthetic sensitivity to drought is a fundamental constraint on land‐plant evolution and ecosystem function. However, little is known about how the sensitivity of photosynthesis to nonstomatal limitations varies among species in the context of phylogenetic relationships. Using saplings of 10 Eucalyptus species, we measured maximum CO₂‐saturated photosynthesis using A–c_i curves at several different leaf water potentials (ψ_leaf) to quantify mesophyll photosynthetic sensitivity to ψ_leaf (MPS), a measure of how rapidly nonstomatal limitations to carbon uptake increase with declining ψ_leaf. MPS was compared to the macroclimatic moisture availability of the species’ native habitats, while accounting for phylogenetic relationships. We found that species native to mesic habitats have greater MPS but higher maximum photosynthetic rates during non‐water‐stressed conditions, revealing a trade‐off between maximum photosynthesis and drought sensitivity. Species with lower turgor loss points have lower MPS, indicating coordination among photosynthetic and water‐relations traits. By accounting for phylogenetic relationships among closely related species, we provide the first compelling evidence that MPS in Eucalyptus evolved in an adaptive fashion with climatically determined moisture availability, opening the way for further study of this poorly explored dimension of plant adaptation to drought.