Genetic studies of Domesticated-Weed-Wild Complexes (DWWC) have typically focused on one-way introgression of crop alleles into wild or weedy populations, with little consideration of the entire natural ecosystem. In Sri Lanka, DWWC is diverse, comprising six evolutionarily discrete groups in the genus Oryza. Using 33 neutral simple sequence repeat (SSR) loci, we characterized six Oryza groups to understand the genetic background and evolution of DWWC components. Our analysis found that Oryza groups have large population sizes and high inter-group long-term gene flows. Asymmetric gene flows were found between wild and weedy rice groups, but the rare alleles shared among DWWC components provide additional evidence for extensive and enduring exchange, highlighting the dynamic nature of this complex genetic admixture among different Oryza lineages. We found high genetic diversity at the population and species levels due to mixed DWWC components over the generations. Weedy rice types exhibit genetic incorporation through admixture from both crop and wild species, highlighting the multi-way genetic transfer in the evolution of weedy rice types. Our findings support the idea that the DWWC is an integrated complex in the Sri Lankan rice ecosystem and that its weedy rice has multiple origins, including de-domestication via feralization of cultivated rice, inter-varietal hybridization among distinct cultivated rice types, adaptation, and invasion of rice cultivation areas by wild Oryza species, and hybridization events between crop and wild rice populations. Abandoned rice domesticates can also evolve into weedy forms with less intimate human relationships and contaminate the rice ecosystem.