This study evaluates the extent to which genetic differences among host individuals from the same species conditions the evolution of a plant RNA virus. We performed a three-fold replicated evolution experiment in which Tobacco etch potyvirus isolate At17b (TEV-At17b), adapted to Arabidopsis thaliana ecotype Ler-0, was serially passaged in five genetically heterogeneous ecotypes of A. thaliana. After 15 passages we found that evolved viruses improved their fitness, showed higher infectivity and stronger virulence in their local host ecotypes. The genome of evolved lineages was sequenced and putative adaptive mutations identified. Host-driven convergent mutations have been identified. Evidences supported selection for increased translational efficiency. Next, we sought for the specificity of virus adaptation by infecting all five ecotypes with all 15 evolved virus populations. We found that some ecotypes were more permissive to infection than others, and that some evolved virus isolates were more specialist/generalist than others. The bipartite network linking ecotypes with evolved viruses was significantly nested but not modular, suggesting that hard to infect ecotypes were infected by generalist viruses whereas easy to infect ecotypes were infected by all viruses, as predicted by a gene-for-gene model of infection.