Significance Viruses are seen as selfish pathogens that harm their hosts to ensure their own survival. However, metagenomic studies are drawing a new picture in which viruses are present everywhere and not always associated to diseases. A classic observation in plant pathology is that the outcome of infection depends on environmental conditions. Here, using experimental evolution, we show that the relationship between a plant virus and its natural host can evolve from pathogenic to mutualistic under severe drought conditions. While viral strains evolved in normal watering conditions increased their virulence, drought-evolved viral strains confer plants with greater resistance to drought. We show that this transition to mutualism depends on a complex reorganization of hormone-induced signaling pathways and changes in gene expression.