Economically important cacao (Theobroma cacao Linnaeus 1753) plantations in South East Asia and Papua New Guinea (PNG) are significantly affected by the cocoa pod borer (CPB) moth. Species identity of the pest is attributed to Conopomorpha cramerella (Snellen 1904), a gracillariid moth endemic to Australasian and Oriental tropic regions that has evolved a host preference for introduced cacao. Suspected presence of cryptic CPB biotypes is largely unsupported by earlier genetic work but remains a concern to organisations developing species‐specific lure and/or control tools for managing this pest. We report the use of DNA barcoding to investigate population and species genetic diversity of CPB infecting cacao plantations in PNG at the eastern periphery of the pest's distribution. DNA barcodes from 94.4% of 179 moths from three disjunct PNG provinces (East Sepik, Bougainville and East New Britain) matched to reported C. cramerella sequence accessions. Genetic diversity among C. cramerella in PNG was limited to four closely related haplotypes, two of which were common in PNG and have previously been reported in the Malay Archipelago at different frequencies. We found evidence of significant population genetic structure between mainland and eastern offshore PNG provinces marked by a reduction of genetic diversity at the offshore provinces. We suggest C. cramerella populations in these offshore island provinces likely arose recently from a genetically depauperate cohort of founders from western sources. Ten moths were genetically unmatched to C. cramerella. Of these, six incidentally captured and degraded adults had novel unmatched DNA barcodes. Four larvae infesting cacao pods were genetically matched to Thaumatotibia zophophanes (Turner 1946) (Lepidoptera: Tortricidae) and an undefined Conopomorpha species distantly related to C. cramerella. The extent to which these two additional moth species affect the cacao industry in PNG (and potentially elsewhere) remains unknown. However, their low representation here (<2.3% of samples) indicates they may be of lesser prominence than the widespread C. cramerella. Nevertheless, organisations designing and/or implementing CPB controls tailored specifically for C. cramerella will need to ensure empirical evidence of control efficiency is monitored with respect to species identity of the captured pests.