The evolution and diversification of ssRNA plant viruses are often examined under reductionist conditions that ignore potentially much wider biotic interactions. The host range of a plant virus is central to interactions at higher levels that are organized by both fitness and ecological criteria. Here we employ a strategy to minimize sampling biases across distinct plant communities and combine it with a high‐throughput sequencing approach to examine the influence of four habitats on the evolution of Watermelon mosaic virus (WMV). Local, regional and global levels of genetic diversity that correspond to spatial and temporal extents are used to infer haplotype relationships using network and phylogenetic approaches. We find that the incidence and genetic diversity of WMV were structured significantly by host species and habitat type. A single haplotype that infected 11 host species of a total of 24 showed that few constraints on host species use exist in the crop communities. When the evolution of WMV was examined at broader levels of organization, we found variation in genetic diversity and contrasting host use footprints that broadly corresponded to habitat effects. The findings demonstrated that nondeterministic ecological factors structured the genetic diversity of WMV. Habitat‐driven constraints underlie host use preferences.