Aedes albopictus (Skuse, 1894) is a mosquito vector raising global health concerns owing to its transmission of dengue, Zika, and chikungunya viruses.This vector accounts for a large proportion of the Korean mosquito community; however, autochthonous clinical cases resulting from this species remain unreported in South Korea.This study aimed to examine the geographical genetic variations and sources of Ae. albopictus populations in South Korea exclusively on the basis of COI gene analysis from 292 samples collected from 37 localities in 2016–2018 and 290 reference sequences from GenBank. Thirty-eight haplotypes were identified among the 292 Ae. albopictus samples, with H1 (n = 190, 65.1%), H29 (n = 24, 8.22%), and H32 (n = 24, 8.22%) being the most common and widely distributed haplotypes in the mainland, southern coastal region, and Jeju Island, respectively. In general, high haplotype (≥0.5; 44.7%) and low nucleotide (≤0.00148 max.) diversity were observed in these populations. Based on eight regional groups, results of neutral tests and a mismatch analysis supported demographic expansions after bottlenecks. Furthermore, analysis of molecular variance, F_ST, and K2P distance showed that Gyeongsangnam-do, Jeju Island, and mainland groups were genetically differentiated. Haplotype network and phylogenetic analyses revealed that the sources of the main haplotypes are related to strains from other countries.The current findings need to be validated with additional sampling from heterogeneous habitats and different genetic markers. However, our results suggest that haplotype changes should be closely monitored for efficient vector surveillance and control.