Leaf CO2 uptake (A) in C4 photosynthesis is limited by the maximum apparent rate of PEPc carboxylation (Vpmax) at low intercellular [CO2] (ci) with a sharp transition to a ci‐saturated rate (Vmax) due to co‐limitation by ribulose‐1:5‐bisphosphate carboxylase/oxygenase (Rubisco) and regeneration of PEP. The response of A to ci has been widely used to determine these two parameters. Vmax and Vpmax depend on different enzymes but draw on a shared pool of leaf resources, such that resource distribution is optimized, and A maximized, when Vmax and Vpmax are co‐limiting. We collected published A/ci curves in 49 C4 species and assessed variation in photosynthetic traits between phylogenetic groups, and as a function of atmospheric [CO2]. The balance of Vmax‐Vpmax varied among evolutionary lineages and C4 subtypes. Operating A was strongly Vmax‐limited, such that re‐allocation of resources from Vpmax towards Vmax was predicted to improve A by 12% in C4 crops. This would not require additional inputs but rather altered partitioning of existing leaf nutrients, resulting in increased water and nutrient‐use efficiency. Optimal partitioning was achieved only in plants grown at pre‐industrial atmospheric [CO2], suggesting C4 crops have not adjusted to the rapid increase in atmospheric [CO2] of the past few decades.