Common ash (Fraxinus excelsior L.) is a tree species of significant ecological and economic importance that has suffered a devastating decline since the 1990s in Europe. Native ash species are being threatened by the alien invasive fungus Hymenoscyphus fraxineus, which causes ash dieback. The main goal of the study was to develop markers for traits related to tolerance to ash dieback and to investigate whether genotypes selected for tolerance were genetically different from susceptible wild populations. We phenotyped 326 ash trees from Sweden for disease severity and genotyped them using 63 amplicon-derived single-nucleotide polymorphism (SNP) markers derived from genes in 40 scaffolds spanning 8 MB in total, which represents approximately 1% of the ash genome. We used a mixed linear model to test for an association between genotypic variation at these loci and disease severity of ash. In total, two SNPs were found to have significant associations. One non-synonymous SNP associated with the disease severity of ash was found in a gene predicted to encode a subtilisin-related peptidase S8/S53 domain. A second marginally significant marker was associated with an LRR gene. Our results demonstrate an inexpensive time-effective method for generating genomic data that could have potential for use in future tree breeding programs and provide information for marker-assisted selection. Our study also showed a low differentiation between genotypes selected for disease tolerance and the wild population of ash representing a range of susceptibilities to ash dieback, indicating opportunities for further selection without significantly losing genetic diversity in the ash population.