Key physiological traits of plants, such as transpiration and stomatal conductance, are usually studied under steady-state conditions or modeled using only a few measured data points. Those measurements do not reflect the dynamic behavior of the plant in response to field conditions. To overcome this bottleneck, we used a gravimetric functional phenotyping platform and a reverse-phenotyping method to examine the dynamic whole-plant water regulation responses of tomato introgression lines and compared those responses with several years of yield performance in commercial fields. Ideotype lines had highly plastic stomatal conductance and high abaxial to adaxial stomatal density ratios and the size of their stomatal apertures peaked early in the day under water-deficit conditions. These traits resulted in dynamic daily water-use efficiency, which allowed for the rapid recovery of transpiration when irrigation was resumed after a period of imposed drought. We found that stomatal density, the abaxial to adaxial stomatal density ratio and the time of maximum stomatal apertures are crucial for plant adaptation and productivity under drought stress conditions. Abaxial stomatal density was also found to be strongly correlated with the expression of the stomatal-development genes SPCH and ZEP. This study demonstrates how a reverse functional phenotyping approach based on field yield data, continuous and simultaneous whole plant waterbalance measurements and anatomical examination of individual leaves can help us to understand and identify dynamic and complex yield-related physiological traits.