The European crabapple Malus sylvestris, a crop wild relative of Malus domestica, is a major contributor to the cultivated apple genome and represents a potential source of interesting alleles or genes, particularly pest resistance traits. An original approach was used to explore the trophic interaction between M. sylvestris populations and its pest, the rosy apple aphid (Dysaphis plantaginea). Using 13 microsatellite markers, population genetic structure and level of crop-to-wild introgressions were inferred between M. sylvestris seedlings from three sites in Europe (Denmark, France, Romania), and M. domestica seedlings. Genetically characterized plants were also used to analyze aphid feeding behavior and fitness parameters. First, aphids submitted to two genetically close M. sylvestris populations (the Danish and French) exhibited similar behavioral parameters, suggesting similar patterns of resistance in these host plants. Second, the Romanian M. sylvestris population was most closely genetically related to M. domestica. Although the two plant genetic backgrounds were significantly differentiated, they showed comparable levels of sensitivity to D. plantaginea infestation. Third, aphid fitness parameters were not significantly impacted by the host plant's genetic background. Finally, crop-to-wild introgression seemed to significantly drive resistance to D. plantaginea independent of host plant population genetic structure, with hybrids being less suitable hosts.