Watermelon mosaic virus (WMV; genus Potyvirus, family Potyviridae) is responsible for serious cucurbit yield losses worldwide. Different WMV genetic groups have been characterized so far. Among these, the "classical" (CL) group has been present in the Mediterranean basin for 40 years, whereas the "emergent" (EM) group includes isolates that are associated with more-severe symptoms observed since 2000. Information on the spatial and temporal evolution of WMV isolates in Italy is currently sparse. In this study, 39 WMV isolates samples collected in different regions over the last two decades were analysed at two different genomic regions that are known to be highly variable and contain recombination breakpoints. Most of the isolates collected between 2002 and 2009 were found to belong to the CL group, whereas the isolates from 2012 onwards were classified as EM, indicating that EM isolates have progressively displaced the CL population in Italy. Although genetic variability was observed within both CL and EM groups and recombinant isolates were detected, no positive selection or haplotype geographic structure were inferred. This suggest that the shift from CL to EM populations was likely due to multiple introductions of EM isolates in different regions of Italy rather than from genetic differentiation of local populations. The progressive increase in prevalence of the highly virulent EM populations is a serious concern because of their symptom severity, and the presence of multiple EM variants that include recombinants necessitates new efforts to develop durable control strategies.