Following its introduction to China, Casuarina equisetifolia rapidly adapted to its new habitat and was extensively cultivated as a crucial tree species for coastal shelterbelts. However, the systematic classification of Chinese landraces remains controversial and the mechanism underlying the rapid adaptation of this species in China remains unknown. To understand more fully the phylogenetic history and adaptation mechanisms of C. equisetifolia, 66 samples were collected from Chinese landraces and five from other potentially related provenances. Single-nucleotide polymorphisms were detected through genotyping-by-sequencing and used for genetic structural analysis and genome comparison. The genetic structures of the Chinese landrace samples were found to be similar or equivalent to those of C. equisetifolia from Southeast Asia; however, admixed structures between C. equisetifolia and Casuarina glauca were also identified, suggesting that spontaneous and frequent interspecific introgression or hybridization had occurred among the Chinese landraces. Genomic variation associated with pathogen–plant interactions was detected between natural provenances and Chinese founder populations along migration pathways. Furthermore, integrated signals were detected in hybrids, including secondary metabolite synthesis from C. glauca, as well as growth regulation and metabolic processes from C. equisetifolia, providing preliminary insights into adaptive mechanisms during the introduction process. These findings improve our knowledge of the phylogenetic history of Casuarina landraces in China, and may enhance the efficiency of domestication and breeding programs.