The incidence and geographic range of Dothistroma septosporum, a serious foliar pathogen of pine, has increased dramatically in central Europe in the last three decades. In Poland, it was first detected in 1990, and by the mid-2010s became established throughout the country, meaning the population of D. septosporum in Poland is relatively young. In this study we analysed site populations of the pathogen in Poland using highly variable microsatellite markers in order to identify the genetic signatures of a recent migration and to track the mode of its introduction. As a result, we found that in Poland the population of D. septosporum is highly structured, the strongest division occurring between a portion of isolates from south-central Poland, including the original outbreak site, and the isolates from the rest of the country. Further genetic structure allowed identification of population clusters specific to particular regions of Poland. Random mating tests show that some population groups have a much lower tendency to reproduce sexually than others, a factor that helps maintain the strong population structure observed. Such a pattern of diversity indicates multiple independent introduction events/migration waves: a single introduction, probably human-mediated, at the original outbreak site, and at least two waves representing a general shift in the distribution of D. septosporum as a consequence of natural spread, resulting in most of the local populations having similar diversity parameters.