During the last century, several forest calamities has been caused by host shifts where an introduced fungus has become a severe pathogen on a native species that lacked co-evolutionary history with the new pathogen. This is considered to be the case for the European ash (Fraxinus excelsior) that in recent decades has become severely damaged throughout most of its natural distribution area by the introduced Asian ascomycete Hymenoscyphus fraxineus. Fortunately, genetic variation in resistance against the novel pathogen in Europe was identified early in the epidemic, and a substantial body of research has since focused on understanding the genetics of this resistance with the vision to promote resilience of ash forest based on wise genetic management practices. Here, we review knowledge obtained from common garden trials, inoculation tests, in situ field studies of mature ash forests, analysis of microbiomes, genomes, transcriptomes and analysis in relation to survival and reproductive fitness. Based on present the knowledge, we discuss how genetic considerations can be integrated into the management of natural and planted ash forests to enhance and protect their resistance and evolutionary resilience.