The capacity of plants to fix carbon is ultimately constrained by two core plant attributes: photosynthetic biochemistry and the conductance to CO2 diffusion from the atmosphere to sites of carboxylation in chloroplasts, predominantly stomatal conductance. Analysis of fossilized plant remains shows that stomatal density (number per unit area, D) and size (length by width, S) have fluctuated widely over the Phanerozoic Eon, indicating changes in maximum stomatal conductance. Parallel changes are likely to have taken place in leaf photosynthetic biochemistry, of which maximal rubisco carboxylation rate, Vcmax is a central element. We used measurements of S and D from fossilized plant remains spanning the last 400 Myr (most of the Phanerozoic), together with leaf gas exchange data and modeled Phanerozoic trends in atmospheric CO2 concentration, [CO2]a, to calibrate a [CO2]a-driven model of the long-term environmental influences on S, D and Vcmax. We show that over the Phanerozoic large changes in [CO2]a forced S, D and Vcmax to co-vary so as to reduce the impact of the change in [CO2]a on leaf CO2 assimilation for minimal energetic cost and reduced nitrogen requirements. Underlying this is a general negative correlation between S and D, and a positive correlation between water-use efficiency and [CO2]a. Furthermore, the calculated steady rise in stomatal conductance over the Phanerozoic is consistent with independent evidence for the evolution of plant hydraulic capacity, implying coordinated and sustained increase in gas exchange capacity and hydraulic capacity parallel long-term increases in land plant diversity.