Technical Abstract: Weedy rice is a significant problem in cultivated rice fields throughout the world, and is an emerging threat in regions where it was previously absent. Prior research has classified weedy rice as the same species as Asian cultivated rice (Oryza sativa L.). This close genetic relationship makes control of the weed particularly difficult. We use genome-wide patterns of single nucleotide polymorphism (SNP) variation in a broad geographic sample of weedy, domesticated, and wild Oryza samples to infer origin and demographic processes influencing weed evolution. We found greater population structure than has been previously reported for U.S. weedy rice, and that multiple, genetically divergent populations have separate origins. The two main U.S. weedy rice populations are largely differentiated morphologically, and share a genetic background with cultivated O. sativa varieties not grown commercially in the U.S., suggesting an origin from domesticated ancestors. Hybridization between weedy groups and between weedy rice and local crops has played a small, but detectable role in U.S. weedy rice evolution. Demographic simulations indicate differences among the main weedy groups in the impact of bottlenecks on their establishment in the U.S., and differences in the timing of divergence from their cultivated relatives.