Watermelon mosaic virus (WMV) is a major plant pathogen, infecting over 170 plant species, including cucurbits and legumes. Though mostly propagated locally by aphids in a non-persistent manner, long-range dispersal can occur through human-induced plant or vector movements. Understanding patterns of local and global spread of WMV is crucial to help formulate adequate control strategies. We used phylodynamic methods based on partial and whole-genome sequences collected in France between 2000 and 2017 to reconstruct the introduction of new lineages in the past 30 years and their subsequent diffusion in the country. We identified at least 11 different introduction events, hailing from different parts of the global diversity of WMV, highlighting the critical role international exchanges play in the spread of plant pathogens. For three of these lineages, we estimated the time and location of their introduction in the mid-1990s in the south of France and the speed at which they spread in this specific landscape. We also showed that the highly recombinogenic nature of WMV, as with most potyviruses, makes the use of whole genomes necessary to classify these viruses on a global scale and must be taken into consideration to reconstruct viral evolutionary history. Our results demonstrate how genomic sequencing of plant viruses can help reconstruct specific viral outbreaks and understand global circulation patterns of plant pathogens.