Abstract Common ash ( Fraxinus excelsior ) is under intensive attack from the invasive alien pathogenic fungus Hymenoscyphus fraxineus , causing ash dieback at epidemic levels throughout Europe. Previous studies have found significant genetic variation among clones in ash dieback susceptibility and that host phenology, such as autumn yellowing, is correlated with susceptibility of ash trees to H. fraxineus ; however, the genomic basis of ash dieback tolerance in F. excelsior remains poorly understood. Here, we integrate quantitative genetics and genome-wide association analyses with machine learning to reveal the genetic architecture of ash dieback tolerance and its relationship to phenological traits in F. excelsior populations in six European countries (Austria, Denmark, Germany, Ireland, Lithuania, Sweden). We use whole-genome sequencing of 486 F. excelsior genotypes to confirm the genotypic correlation between crown damage caused by ash dieback and intensity of autumn leaf yellowing within multiple sampling sites. Although, our results suggest that the examined traits are polygenic, a relatively small number of single nucleotide polymorphisms (SNPs) explained a large proportion of the variation in both disease tolerance and autumn leaf yellowing. We could explain up to 63% (based on 9155 unlinked SNPs) of variation in individual response to ash dieback crown damage and up to 72% (based on 3740 unlinked SNPs) of variation in autumn yellowing. We identified eight SNPs encoding non-synonymous substitutions, of which those with the highest predictive power were located within genes related to plant defence (pattern triggered immunity, pathogen detection) and phenology (regulation of flowering and seed maturation, auxin transport). Overall, our results provide insights of a multifaceted defence response, according to which a combination of direct defence mechanisms and phenological avoidance of pathogen spread constitute tolerance to ash dieback.< Réduire