The ecologically and culturally vital tree species, ʻōhiʻa lehua (Metrosideros polymorpha), is threatened by the fungal pathogens Ceratocystis lukuohia and Ceratocystis huliohia, the causal agents of the disease complex called Rapid ʻŌhiʻa Death (ROD). Four invasive ambrosia beetle (Coleoptera: Curculionidae: Scolytinae) species in the Xyleborini tribe colonize ROD Ceratocystis-infested ‘ōhiʻa and produce inoculum through their frass; however, the potential for direct transmission of the ROD fungi by these beetles was unknown. We fulfilled Leach's rules to support insect transmission of ROD by documenting the visitation of these ambrosia beetles to healthy ‘ōhiʻa trees, culturing C. lukuohia and C. huliohia from the ROD-associated beetles using three different collection methods at multiple study sites, and challenging healthy ʻōhiʻa seedlings with beetles that were exposed to both C. lukuohia and C. huliohia cultures. We documented all four invasive ROD-associated ambrosia beetle species including Xyleborinus saxesenii, Xyleborus affinis, Xyleborus ferrugineus, and Xyleborus perforans to regularly visit healthy ʻōhiʻa trees on sticky traps. Viable Ceratocystis propagules were isolated from all species, and C. lukuohia was most commonly isolated of the two ROD-causing fungi. Consistently across all collection techniques, ROD Ceratocystis spp. were detected on just under 3% of all assayed beetles, with the highest detection rate from X. affinis. All four beetle species were capable of directly transmitting both pathogens to healthy ʻōhiʻa seedlings with a high rate of transfer. Ceratocystis spp. are highly virulent pathogens in trees, and a single inoculation can result in tree death, therefore any direct transmission is a cause for concern. After meeting the criteria of Leach's rules, we propose that Xi. saxesenii, X. affinis, X. ferrugineus, and X. perforans are vectors of C. lukuohia and C. huliohia, particularly in areas of high ROD pressure and tree stress.