For agricultural pests capable of attacking different plant species, crop distribution and selection pressure imposed by insecticide use are two key constraints imposed on their evolutionary trajectory. Here, we assessed the contribution of host-based genetic differentiation to the dynamics of resistance alleles to three insecticide modes of action in Myzus persicae. This major aphid pest is infamous for its ability to resist to multiple insecticides. Two distinct samplings were conducted: reference sampling on identified crops and continuous random sampling for 7 years using a suction trap. All aphids were genotyped at 14 microsatellite markers and four insecticide-resistant loci. We analyzed the genetic structure of these populations using an individual-centered approach. Four well-defined genetic clusters were found in the aerial samples, three of which could be linked to specific crops. We found a sharp differentiation between peach and herbaceous individuals. Within the individuals sampled on herbaceous hosts, two distinct genetic clusters were identified, one of which seems to be more strongly associated with tobacco. The fourth group was only found in the aerial samples and display strong genetic difference with other groups. The 4-loci resistance genotypes showed a strong association with the four genetic clusters, indicative of barriers to the spread of insecticide resistances. The 7-year continuous random sampling revealed a rapid turnover in aphid genotypes and associated insecticide resistance patterns. This study highlights the importance of considering landscape-scale population structure to identify the risk of emergence and spread of insecticide resistance for a particular crop.