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Ambrosia beetles and their microbial communities, housed in specialized structures termed mycangia, represent one of the oldest and most diverse systems of mutualism and parasitism described thus far. Comprised of core filamentous fungal members, but also including bacteria and yeasts, the mycangia represent a unique adaptation that allows beetles to store and transport their source of nutrition. Although perhaps the most ancient of "farmers," the nature of these interactions remains largely understudied, with the exception of a handful of emerging pathosystems, where the fungal partner acts as a potentially devastating tree pathogen. Such virulence is often seen during "invasions," where (invasive) beetles carrying the fungal symbiont/plant pathogen expand into new territories and presumably "naïve" trees. Here, we summarize recent findings on the phylogenetic relationships between beetles and their symbionts and advances in the developmental and genetic characterization of the mechanisms that underlie insect-fungal-plant interactions. Results on genomic, transcriptomic, and metabolomic aspects of these relationships are described. Although many members of the fungal Raffaelea-beetle symbiont genera are relatively harmless to host trees, specialized pathosystems including wilt diseases of laurel and oak, caused by specific subspecies (R. lauricola and R. quercus, in the USA and East Asia, respectively), have emerged as potent plant pathogens capable of killing healthy trees. With the development of genetic tools, coupled to biochemical and microscopic techniques, the ambrosia beetle-fungal symbiont is establishing itself as a unique model system to study the molecular determinants and mechanisms that underlie the convergences of symbioses, mutualism, parasitism, and virulence. Key points: • Fungal-beetle symbioses are diverse and ancient examples of microbial farming. • The mycangium is a specialized structure on insects that houses microbial symbionts. • Some beetle symbiotic fungi are potent plant pathogens vectored by the insect. [ABSTRACT FROM AUTHOR]