How rootstocks contribute to the control of scion transpiration under drought is poorly understood. We investigated the role of root characteristics, hydraulic conductance and chemical signals (abscisic acid, ABA) in the response of stomatal conductance (gs) and transpiration (E) to drought in Cabernet Sauvignon (Vitis vinifera) grafted onto drought-sensitive (Vitis riparia) and drought-tolerant (Vitis berlandieri × Vitis rupestris 110R) rootstocks. All combinations showed a concomitant reduction in gs and E, and an increase in xylem sap ABA concentration during the drought cycle. Cabernet Sauvignon grafted onto 110R exhibited higher gs and E under well-watered and moderate water deficit, but all combinations converged as water deficit increased. These results were integrated into three permutations of a whole-plant transpiration model that couples both chemical (i.e., ABA) and hydraulic signals in the modelling of stomatal control. Model comparisons revealed that both hydraulic and chemical signals were important for rootstock-specific stomatal regulation. Moreover, model parameter comparison and sensitivity analysis highlighted two major parameters differentiating the rootstocks: (i) ABA biosynthetic activity and (ii) the hydraulic conductance between the rhizosphere and soil-root interface determined by root system architecture. These differences in root architecture, specifically a higher root length area in 110R, likely explain its higher E and gs observed at low and moderate water deficit.