The increasing fragmentation of forest habitats and the omnipresence of cultivars potentially threaten the genetic integrity of the European wild apple (Malus sylvestris (L.) Mill). However, the conservation status of this species remains unclear in Europe, other than in Belgium and the Czech Republic, where it has been declared an endangered species. The population density of M. sylvestris is higher in the forests of the upper Rhine Valley (France) than in most European forests, with an unbalanced age-structure, an overrepresentation of adults and a tendency to clump. We characterize here the ecology, age-structure and genetic diversity of wild apple populations in the Rhine Valley. We use these data to highlight links to the history of this species and to propose guidelines for future conservation strategies. In total, 255 individual wild apple trees from six forest stands (five floodplain forests and one forest growing in drier conditions) were analysed in the field, collected and genotyped on the basis of data for 15 microsatellite markers. Genetic analyses showed no escaped cultivars and few hybrids with the cultivated apple. Excluding the hybrids, the genetically “pure” populations displayed high levels of genetic diversity and a weak population structure. Age-structure and ecology studies of wild apple populations identified four categories that were not randomly distributed across the forests, reflecting the history of the Rhine forest over the last century. The Rhine wild apple populations, with their ecological strategies, high genetic diversity, and weak traces of crop-to-wild gene flow associated with the history of these floodplain forests, constitute candidate populations for inclusion in future conservation programmes for European wild apple.