Both SH and BHA weedy rice genotypes evolved independently and have distinct genomic composition. Different genetic mechanisms may be responsible for their competitiveness and adaptation to diverse environmental conditions. Two major types of weedy rice are recognized in the USA based on morphology: straw-hull (SH) and black-hull awned (BHA) weedy rice. We performed whole-genome resequencing of a SH weedy rice 'PSRR-1', a BHA weedy rice 'BHA1115', and a japonica cultivar 'Cypress' to delineate genome-wide differences and their relevance to genetics and evolution of weedy attributes. The high-quality reads were uniformly distributed with 82-88% genome coverage. The number of genotype-specific SNPs and InDels was highest in Cypress, followed by BHA1115 and PSRR-1. However, more genes were affected in BHA1115 compared with other two genotypes which is evident from the number of high-impact SNPs and InDels. Haplotype analysis of selected genes involved in domestication, adaptation, and agronomic performance not only differentiated SH from BHA weedy rice and supported evolution of weedy rice through de-domestication, but also validated the function of several genes such as qAn-1, qAn-2, Bh4, Rc, SD1, OsLG1, and OsC1. Several candidate genes were identified for previously reported seed dormancy and seed shattering QTLs. The SH and BHA weedy rice have distinct genomic composition, and the BHA weedy rice likely diverged earlier than SH weedy rice. The accumulation of plant development, reproduction, and defense-related genes in weedy rice possibly helped them to compete, survive, and spread under a wide range of environmental conditions by employing novel and diverse mechanisms. The genomic resources will be useful for both weed management and rice improvement by exploring the molecular basis of key agronomic, adaptive, and domestication attributes.