Watermelon mosaic virus (WMV, genus Potyvirus, family Potyviridae) was reported for the first time in France in 1974, and it is now the most prevalent virus in cucurbit crops. In 2000, new strains referred as ‘emerging’ (EM) strains were detected in South-eastern France. EM strains are generally more severe and phylogenetically distinct from those previously reported in this country and referred as ‘classic’ (CL) strains. Since 2000, EM strains have been progressively replacing CL strains in several areas where they co-exist. In order to explain this rapid shift in virus populations, the biological properties of a set of 17 CL and EM WMV isolates were compared. No major differences were observed when comparing a limited host range including 48 different plant species or cultivars. Only two species were differential; Chenopodium quinoa was systemically infected by CL and not by EM isolates whereas Ranunculus sardous was systemically infected by EM and not by CL isolates. A considerable variability was observed in aphid transmission efficiencies but this could not be correlated to the CL or EM types. Two subsets of five isolates of each group were used to compare aphid transmission efficiencies from single and double (CL–EM) infections using six different cucurbit and non-cucurbit hosts. EM isolates were generally better transmitted from mixed CL–EM infections than CL isolates and CL transmission rates were significantly lower from double than from single infections. Cross-protection was only partial between CL and EM strains leading to frequent double infections, and only a slight asymmetry was observed in cross-protection efficiencies. Since double infections occur very commonly in fields, the preferential transmission of EM from mixed CL–EM infections could be one of the factors leading to the displacement of CL isolates by EM isolates.