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ABSTRACT Herbicide resistance in agricultural weeds has become one of the greatest challenges for sustainable crop production. The repeated evolution of herbicide resistance provides an excellent opportunity to study the genetic and physiological basis of the resistance phenotype and the evolutionary responses to human‐mediated selection pressures.Lolium multiflorumis a ubiquitous weed that has evolved herbicide resistance repeatedly around the world in various cropping systems. We assembled and annotated a chromosome‐scale genome forL. multiflorumand elucidated the genetic architecture of paraquat resistance by performing quantitative trait locus analysis, genome‐wide association studies, genetic divergence analysis and transcriptome analyses from paraquat‐resistant and ‐susceptibleL. multiflorumplants. We identified two regions on chromosome 5 that were associated with paraquat resistance. These regions both showed evidence for positive selection among the resistant populations we sampled, but the effects of this selection on the genome differed, implying a complex evolutionary history. In addition, these regions contained candidate genes that encoded cellular transport functions, including a novel multidrug and toxin extrusion (MATE) protein and a cation transporter previously shown to interact with polyamines. Given thatL. multiflorumis a weed and a cultivated crop species, the genomic resources generated will prove valuable to a wide spectrum of the plant science community. Our work contributes to a growing body of knowledge on the underlying evolutionary and ecological dynamics of rapid adaptation to strong anthropogenic selection pressure that could help initiate efforts to improve weed management practices in the long term for a more sustainable agriculture.