Plants can be subjected simultaneously to abiotic and biotic stresses, such as drought and viral infections. Rewarding effects provided by viruses helping plants to endure abiotic stresses have been reported, underpinning the existence of common molecular networks that regulate the responses towards these stimuli. Recently, begomoviruses causing the tomato yellow leaf curl disease in tomatoes were shown to increase heat and drought tolerance. possibly through the intervention of the viral C4 protein. Here, we elucidate physiological and molecular events underlying the drought tolerance induced in tomato by the tomato yellow leaf curl Sardinia virus (TYLCSV) and by its C4 protein when overexpressed in transgenic tomato plants. Combining the determination of morphometric and physiological parameters and hormone content with transcriptional analysis of genes involved in water stress response and hormone metabolism, we assessed that TYLCSV and the overexpressed C4 protein induce a delay in the onset of stress-related features, improve the water use efficiency, and facilitate a rapid post-rehydration recovery. Specific anatomical and hydraulic traits, rather than biochemical signals, support such increased drought stress resilience. Overall, the priming role exerted by TYLCSV and its C4 protein in the adaptation to abiotic stresses opens new perspectives in the management of the effects of climate change in horticultural crops.