Drought is a major cause of yield loss for crops worldwide. Climate change is predicted to increase global crop losses due to drought through rising temperature and decreased water availability. Virus infection can increase drought tolerance of infected plants compared to non-infected plants; however, the mechanisms mediating virus-induced drought tolerance remain unclear. In this study, we demonstrate Turnip mosaic virus (TuMV) infection increases Arabidopsis thaliana survival under drought compared to uninfected plants. To determine if specific TuMV proteins mediate drought tolerance, we cloned the coding sequence for each of the major viral proteins and generated transgenic A. thaliana that constitutively express each protein. Three TuMV proteins, 6K1, 6K2, and NIa-Pro, enhanced drought tolerance of A. thaliana when expressed constitutively in plants compared to controls. Expression of 6K2 also increased plant biomass relative to controls, but had no impact on root biomass, trichome numbers, or on the number of stomata. While drought induced transcripts related to abscisic acid (ABA) biosynthesis and ABA levels in control plants, compared to under well-watered conditions, there were no changes in ABA or related transcripts in plants expressing 6K2 under drought conditions compared to well-watered. 6K2 expression also conveyed drought tolerance in another host plant, Nicotiana benthamiana, when expressed using a virus over expression construct derived from Foxtail mosaic virus (FoMV). Although the exact mechanisms are still unknown, these results suggest 6K2-induced drought tolerance is ABA-independent and that plant viruses may represent novel sources of drought tolerance for crop plants.