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In this genome-wide association study, we obtained novel insights into the genetic basis of the effect of herbivory or drought stress on the level of resistance against the fungus Botrytis cinerea. In nature, plants function in complex environments where they encounter different biotic and abiotic stresses individually, sequentially or simultaneously. The adaptive response to a single stress does not always reflect how plants respond to such a stress in combination with other stresses. To identify genetic factors that contribute to the plant's ability to swiftly adapt to different stresses, we investigated the response of Arabidopsis thaliana to infection by the necrotrophic fungus B. cinerea when preceded by Pieris rapae herbivory or drought stress. Using 346 natural A. thaliana accessions, we found natural genetic variation in the level of resistance against single B. cinerea infection. When preceded by herbivory or drought stress, the level of B. cinerea resistance was differentially influenced in the 346 accessions. To study the genetic factors contributing to the differential adaptation of A. thaliana to B. cinerea infection under multi-stress conditions, we performed a genome-wide association study supported by quantitative trait loci mapping and fine mapping with full genome sequences of 164 accessions. This yielded several genes previously associated with defense to B. cinerea and additional candidate genes with putative roles in the plant's adaptive response to a combination of herbivory, drought and B. cinerea infection.