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In plants, introgression of genetic resistances is a proven strategy for developing new resistant lines. While host proteins involved in genome replication and cell-to-cell movement are widely studied, other cellular mechanisms responsible for viral infection remain underestimated. Endosomal sorting complexes required for transport (ESCRT) proteins play a key role in membrane trafficking in plants and are involved in the replication of several plant RNA viruses. We have demonstrated for the first time the role of the ESCRT protein CmVPS4 as a novel susceptibility factor for the Potyvirus watermelon mosaic virus (WMV) in melon. By screening a worldwide collection of melons, we identified three different alleles carrying non-synonymous substitutions in CmVps4. Two of these alleles were shown to be associated with WMV resistance. Using a complementation approach, we demonstrated that resistance is due to a single non-synonymous substitution in the allele CmVps4^P30R. This work opens up new avenues of research on a new family of host factors required for virus infection and new targets for resistance.