Population genetic studies of insect pests enhance our ability to anticipate problems in agroecosystems, such as pest outbreaks, insecticide resistance, or expansions of the host range. This study focuses on geographic distance and host plant selection as potential determinants of genetic differentiation of the carrot weevil Listronotus oregonensis, a major pest of several apiaceous crops in North America. To undertake genetic studies on this species, we assembled the first complete genome sequence for L. oregonensis. Then, we used both haplotype discrimination with mitochondrial DNA (mtDNA) and a genotyping‐by‐sequencing (GBS) approach to characterize the genetic population structure. A total of 220 individuals were sampled from 17 localities in the provinces of Québec, Ontario, Nova Scotia (Canada), and the state of Ohio (USA). Our results showed significant genetic differences between distant populations across North America, indicating that geographic distance represents an important factor of differentiation for the carrot weevil. Furthermore, the GBS analysis revealed more different clusters than COI analysis between Québec and Nova Scotia populations, suggesting a recent differentiation in the latter province. In contrast, we found no clear evidence of population structure associated with the four cultivated apiaceous plants tested (carrot, parsley, celery, and celeriac) using populations from Québec. This first characterization of the genetic structure of the carrot weevil contributes to a better understanding of the gene flow of the species and helps to adapt local pest management measures to better control this agricultural pest.