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Cycas sect. Asiorientales comprises two East Asian island species, Cycas revoluta and C. taitungensis. Shared genetic polymorphism between these two species has been reported, indicating that interspecific gene flow may have occurred. In this study, the delimitation of these two species was clarified with two other Cycas sections, Stangerioides and Panzhihuaensis. To examine the degree of genetic admixture, model-based Bayesian clustering analysis and isolation-with-migration analysis were conducted using multilocus genome scans and nuclear DNA sequence data, respectively. The paraphyletic relationship between these two cycads, as inferred from multilocus markers, confirms previous results wherein the paraphyletic relationship was inferred from plastid DNA. The ancient gene flow inferred by isolation-with-migration analysis suggests that the mild genetic admixture observed cannot just be explained by recent introgression. Instead, consideration should be given to past secondary contacts during repeated land bridge formation between Taiwan and Ryukyus in the Quaternary ice ages.