The intense and unidirectional selection pressure caused by the massive deployment of resistant plants can result in rapid adaptation of pathogen populations1. Such rapid evolution was documented for the poplar rust fungus. In 1994, poplar rust populations suddenly overcame the RMlp7 qualitative resistance carried by several poplar cultivars planted widely in Western Europe2,3. This recent event of adaptation from standing genetic variation caused a selective sweep on the rust genome4. We study a 25-year temporal sampling of poplar rust populations to decipher the demographic and evolutionary history of this pathogen while overcoming its host genetic resistance. Using resurrection ecology, we examine phenotypic and genetic variations throughout this adaptive event. Our analyses reveal that a unique and homogeneous genetic group overcame RMlp7 resistance and replaced the ancestral genetic group within five years. We then use forward simulations to 1) understand the interplay between demography and genetic evolution underpinning the rapid evolution of poplar rust populations, and 2) disentangle the polymorphism signatures of selection from that of stochastic processes due to demographic changes. We show high stochasticity in evolutionary trajectories with the notable effect of evolutionary rescue scenarios on polymorphism signatures. Finally, we integrate our simulator in an Approximate Bayesian approach (ABC) to infer the demographic and selection parameters from temporal genetic data. Our statistical framework coupling modelling with temporal data is powerful to understand recent events of rapid adaptation. 1 Saubin et al. DOI:10.24072/pcjournal.10 2 Louet et al. DOI:10.1111/mec.16294 3 Persoons et al. DOI:10.1111/mec.13980 4 Persoons et al. DOI:10.1093/gbe/evab279