Trichonephila clavata L. Koch, 1878, an East Asian species renowned for its long-distance ballooning dispersal, has recently drawn attention as an invasive species following its introduction into the southeastern United States. However, few population genetic studies have been undertaken to investigate population genetic diversity and structure which will be helpful for its management. Here, we examined ten populations of T. clavata on the Korean Peninsula using mitochondrial COI and genome-wide SNP data to broadens the understanding of genetic and demographic processes of the species. Our results revealed: (1) high genetic diversity in COI but relatively low diversity in SNPs; (2) the presence of three genetic lineages detected by both markers; (4) population expansion in each COI genetic lineage and constant population size in each SNP genetic lineage; and (5) stepwise lineage divergence estimated based on COI and lineage divergence with admixture event based on SNPs. These findings suggest that multiple factors, which are ballooning dispersal, demographic dynamics and geological event, may play a pivotal role in shaping population genetic patterns with geographic co-occurrence among the lineages. Consequently, this study provides insights into the genetic architecture of natural populations and offers a valuable baseline for understanding the population genetic pools of invasive populations of this species.