Identifying the invasion routes and determining the origin of new outbreaks of invasive species are of crucial importance if we are to understand the invasion process, improve or establish regulatory measures and, potentially, limit the damage. We focused here on the invasion of Europe by the pinewood nematode (PWN), Bursaphelenchus xylophilus (Steiner & Buhrer, 1934; Nickle 1970; Nematoda: Aphelenchoididae), a major pest of forest ecosystems, native to North America and already invasive in Asia since the beginning of the twentieth century. We evaluated the genetic diversity and structure of worldwide field PWN samples by classical and Bayesian population genetics methods to determine the source of the European invasive populations and the number of introduction events in Europe. We found (1) a very strong spatial genetic structure in native PWN populations, (2) a very low level of polymorphism in each of the invaded areas and (3) contrasted results concerning the origin of European invasive populations. Our findings provide evidence for: (1) a large effect of genetic drift on the biological cycle of the PWN, due to intense demographic bottlenecks during tree infections, not compensated for by effective dispersal of its vector; (2) a single introduction event for each of the invaded areas in Japan and Europe and a small effective size for the introduced populations and (3) a mainland Portuguese origin for PWN populations from Madeira. However, more sophisticated methods of invasion route inference and broader sampling are required to conclusively determine the origin of the European outbreak.