The arbovirus vector Aedes albopictus (Asian tiger mosquito) is common throughout the Indo-Pacific region, where most global dengue transmission occurs. We analysed population genomic data and tested for cryptic species in 160 Ae. albopictus sampled from 16 locations across this region. We found no evidence of cryptic Ae. albopictus but found multiple intraspecific COI haplotypes partitioned into groups representing three Asian lineages: East Asia, Southeast Asia and Indonesia. Papua New Guinea (PNG), Vanuatu and Christmas Island shared recent coancestry, and Indonesia and Timor-Leste were likely invaded from East Asia. We used a machine learning trained on morphologically sexed samples to classify sexes using multiple genetic features and then characterized the w AlbA and w AlbB Wolbachia infections in 664 other samples. The w AlbA and w AlbB infections as detected by qPCR showed markedly different patterns in the sexes. For females, most populations had a very high double infection incidence, with 67% being the lowest value (from Timor-Leste). For males, the incidence of double infections ranged from 100% (PNG) to 0% (Vanuatu). Only 6 females were infected solely by the w AlbA infection, while rare uninfected mosquitoes were found in both sexes. The w AlbA and w AlbB densities varied significantly among populations. For mosquitoes from Torres Strait and Vietnam, the w AlbB density was similar in single-infected and superinfected ( w AlbA and w AlbB) mosquitoes. There was a positive association between w AlbA and w AlbB infection densities in superinfected Ae. albopictus . Our findings provide no evidence of cryptic species of Ae. albopictus in the region and suggest site-specific factors influencing the incidence of Wolbachia infections and their densities. We also demonstrate the usefulness of SNPs as sex-specific mosquito markers. The results provide baseline data for the exploitation of Wolbachia -induced cytoplasmic incompatibility (CI) in dengue control.