In 2001, although target site resistance against pyrethroids was wide-spread in clonal populations of Myzus persicae on oilseed rape in France (kdr), target site resistance against carbamates was rare. Starting in 2005, control failure by carbamates appeared. The current study was designed to document changes in insecticide-resistant genotype frequencies in France during the last decade. Two resistant genotypes (RGs) were dominant in populations in 2009–2010: RG1 with the kdr 1014F allele (16%), RG2 with the MACE 431F allele and the atypical s-kdr 918L allele (83%). The widespread prevalence of RG2 suggests that a substantial shift has occurred (allele 431F in <2% individuals in 2001) presumably in response to agrichemicals. Analysis of neutral markers revealed that 2009–2010 populations were composed of two differentiated genetic pools (instead of one in 2001) and that RG2 was found in two divergent superclones of M. persicae. Possible explanations for these observed shifts in population structure and especially for the dramatic increase of the double mutant RG2 are discussed.