Weedy rice possesses robust ecological adaptability; however, how this strain originated and gradually formed proprietary genetic features remains unclear. Here, we demonstrate that weedy rice at Asian high latitudes (WRAH) is phylogenetically well-defined and presents unselected genomic spectra in many weedy-cultivated divergence islands. We also explored some novel QTLs for weedy-specific traits and proposed that a genome block in the end of chromosome 1 contributes to rice weediness. On the other hand, we first de novo assembled a high-quality weedy rice genome (WR04-6) to identify the genomic modifications underlying weedy rice evolution. Then, we conducted a comparative genomics study for WR04-6 with other rice reference genomes. Multiple lines of evidence, including demographic scenario comparisons, suggest that differentiation between weedy rice and cultivated rice initiated by genetic improvement of cultivated rice and the essence of weediness was semi-domestication. A plant height model further implied the origin of WRAH as an evolutionary game and indicated that strategy-based selection driven by fitness shaped its genomic diversity.