Rapid ‘Ōhi‘a Death (ROD) is a deadly disease that is threatening the native Hawaiian keystone tree species, ‘ōhi‘a lehua (Metrosideros polymorpha Gaudich). Ambrosia beetles (Curculionidae: Scolytinae) and their frass are hypothesized to play a major role in the spread of ROD, although their ecological niches and frass production within trees and across the landscape are not well understood. We characterized the beetle communities and associated frass production from bolts (tree stem sections) representative of entire individual ‘ōhi‘a trees from multiple locations across Hawai‘i Island by rearing beetles and testing their frass for viable ROD-causing fungi. Additionally, we estimated frass production for three beetle species by weighing their frass over time. We found that Xyleborinus saxesenii (Ratzburg), Xyleborus affinis Eichhoff, Xyleborus ferrugineus (Fabricius), Xyleborus perforans (Wollaston), and Xyleborus simillimus Perkins were commonly found on ROD-infected ‘ōhi‘a and each produced frass containing viable Ceratocystis propagules. The Hawai‘i Island endemic beetle and the only native ambrosia beetle associated with ‘ōhi‘a, X. simillimus, was limited to high elevations and appeared to utilize similar tree heights or niche dimensions as the invasive X. ferrugineus. Viable Ceratocystis propagules expelled in frass were found throughout entire tree bole sections as high as 13 m. Additionally, we found that X. ferrugineus produced over 4× more frass than X. simillimus. Our results indicate the ambrosia beetle community and their frass play an important role in the ROD pathosystem. This information may help with the development and implementation of management strategies to control the spread of the disease.