Following the Red Queen co-evolutionary dynamics, the arms race in a host-parasite system can lead to population extinction. Such an extinction has been described in the poplar – M. larici-populina (poplar rust fungus) pathosystem: a major adaptive event occurred in 1994 with the breakdown of the R7 resistance carried by poplar cultivars widely planted in Western Europe. This resistance breakdown resulted in the emergence and expansion of a genetic group (virulent 7) that replaced the initial avirulent 7 group which predominated previously (Persoons et al, 2017). To understand the genetic basis and the demographic consequences of such an event, we developed a model of the demographic history of M. larici-populina. We selected 79 isolates spanning the date of detection of R7 breakdown, and we detected polymorphisms using whole-genome resequencing. We modelled the ancestry of these genetic groups using Approximate Bayesian Computation, which enabled us to test alternative hypotheses concerning the origin of the virulent 7 population and to estimate key demographic parameters. We used a genome scan approach based on a combination of standard neutrality tests and identified a genomic region showing signatures of a selective sweep, later confirmed by a GWAS approach as the potential location of the avirulence 7 locus. The current acquisition of a new reference genome from an avirulent 7 isolate will help characterizing the genetic basis that led to the virulence 7 emergence.