In fluctuating environments, the kinetics of stomatal opening and closing influence the balance between carbon gain and water loss. Smaller guard cells may respond faster to fluctuating environmental conditions because of their greater surface area for osmolyte flux relative to cell volume. A related hypothesis is that operational stomatal conductance ( g op ) is often well below its theoretical maximum ( g max ) because at this stomatal aperture, guard cell volume is poised to change rapidly with small changes in turgor pressure. We analyzed 2,124 estimates of stomatal closure kinetics in response to an abrupt increase in vapor pressure deficit (VPD) among 29 diverse wild tomato populations in the genus Solanum . Leaves with small guard cells and a lower g op to g max ratio ( f gmax ) closed faster, but explained variation in kinetic parameters at different levels of biological organization. Guard cell size had high phylogenetic heritability and varied relatively little within populations, whereas f gmax varied mostly among individuals and between light intensity treatments. Smaller stomata can be speedier, but only if stomata are held at an aperture where they are responsive to changing turgor pressure. Selection on stomatal speed may influence not only anatomical traits like guard cell size, but also physiological controls on g op .