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Abstract Oak trees are of major economic and ecological importance globally. In England the main oak species is Quercus robur (English oak). Establishment and growth of Q. robur has suffered from the spread of the powdery mildew, a fungal foliar disease, over the past century, which affects trees of all ages. In recent decades, acute oak decline (AOD) has damaged many mature Q. robur populations; this is a complex syndrome in which predisposing environmental factors, a beetle, and four bacterial species have been implicated. Little is known about genetic factors contributing to AOD and mildew symptoms. Here we analyse the population structure of British oak populations using the whole genomes of 1868 oak trees from 78 sites. Retaining 1491 trees exclusively of the species Q. robur , we investigate the genetic component of AOD and mildew susceptibility, and its architecture. Using single nucleotide polymorphism (SNP) based estimates of heritability, we estimate 20.9% of variation in AOD presence is genetically determined. For mildew symptoms, this figure is higher, at 27.8%. Using genome-wide association studies, no SNP markers cross significance thresholds for AOD, but 183 are significant for mildew. Genomic prediction models for AOD and its symptoms, using thousands of loci, give low to moderate accuracies, ranging from 0.187 to 0.617. These results suggest a highly polygenic heritable component of susceptibility to AOD, which is not surprising given the number of biotic and abiotic factors known to contribute to it. In contrast, powdery mildew, caused by a single fungus, has an oligogenic heritable component controlled by fewer loci of large effect. These results could be used to inform breeding programs to develop trees more resistant to AOD and mildew.