Stomatal responses to fluctuating light and CO2 were investigated in Zea mays and Phaseolus vulgaris. Slow-moving stomata can affect carbon gain and water loss by plants during light flecks, under dynamic cloud cover, during alternating windy and calm air conditions (which influence CO2 concentrations and humidity immediately around leaves in plant canopies), at natural CO2 vents, or in growth chambers with imperfect CO2 control. It was found that the frequency of constant-amplitude fluctuations in light and CO2 dramatically affected the time-averaged stomatal conductance in both Zea and Phaseolus. During oscillations in light, average stomatal conductance was driven either above or below that observed at steady state at the average light level, depending on the frequency of the oscillations. Under oscillating CO2, the departure of average stomatal conductance away from that observed at steady state at the average CO2 level was also frequency dependent in both species. Upon cessation of oscillations and return of light or CO2 to the stable median level, stomatal conductance also returned to a steady state, matching that before oscillations were initiated. This work shows that fluctuations in light and CO2, and equally important, their frequency, can be critical in determining time-averaged stomatal conductance under unstable environmental conditions.