Summary Exotic pathogens cause severe damage in natural populations in the absence of coevolutionary dynamics with their hosts. However, some resistance to such pathogens may occur in naive populations. The objective of this study was to investigate the genetics of this so‐called ‘exapted’ resistance to two pathogens of Asian origin (Erysiphe alphitoides and Phytophthora cinnamomi) in European oak. Host–pathogen compatibility was assessed by recording infection success and pathogen growth in a full‐sib family of Quercus robur under controlled and natural conditions. Two high‐resolution genetic maps anchored on the reference genome were used to study the genetic architecture of resistance and to identify positional candidate genes. Two genomic regions, each containing six strong and stable quantitative trait loci (QTLs) accounting for 12–19% of the phenotypic variation, were mainly associated with E. alphitoides infection. Candidate genes, especially genes encoding receptor‐like‐kinases and galactinol synthases, were identified in these regions. The three QTLs associated with P. cinnamomi infection did not colocate with QTLs found for E. alphitoides. These findings provide evidence that exapted resistance to E. alphitoides and P. cinnamomi is present in Q. robur and suggest that the underlying molecular mechanisms involve genes encoding proteins with extracellular signaling functions.