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ABSTRACT Weedy rice is a close relative of cultivated rice (Oryza sativa) that infests rice fields worldwide and drastically reduces yields. To combat this agricultural pest, rice farmers in the southern US began to grow herbicide‐resistant (HR) rice cultivars in the early 2000s, which permitted the application of herbicides that selectively targeted weedy rice without harming the crop. The widespread adoption of HR rice coincided with increased reliance on hybrid rice cultivars in place of traditional inbred varieties. Although both cultivated and weedy rice are predominantly self‐fertilising, the combined introductions of HR and hybrid rice dramatically altered the opportunities and selective pressure for crop‐weed hybridization and adaptive introgression. In this study, we generated genotyping‐by‐sequencing data for 178 weedy rice samples collected from across the rice growing region of the southern US; these were analysed together with previously published rice and weedy rice genome sequences to determine the recent genomic and population genetic consequences of adaptive introgression and selection for herbicide resistance in US weedy rice populations. We find a reshaped geographical structure of southern US weedy rice as well as purging of crop‐derived alleles in some weed strains of crop‐weed hybrid origin. Furthermore, we uncover evidence that related weedy rice strains have made use of different genetic mechanisms to respond to selection. Lastly, we identify widespread presence of HR alleles in both hybrid‐derived and nonadmixed samples, which further supports an overall picture of weedy rice evolution and adaptation through diverse genetic mechanisms.