BackgroundIps typographus(European spruce bark beetle) is the most destructive pest of spruce forests in Europe. As for other animals, it has been proposed that the microbiome plays important roles in the biology of bark beetles. About the bacteriome, there still are many uncertainties regarding the taxonomical composition, insect-bacteriome interactions, and their potential roles in the beetle ecology. Here, we aim to deep into the ecological functions and taxonomical composition ofI. typographusassociated bacteria.ResultsWe assessed the metabolic potential of a collection of isolates obtained from different life stages ofI. typographusbeetles. All strains showed the capacity to hydrolyse one or more complex polysaccharides into simpler molecules, which may provide an additional carbon source to its host. Also, 83.9% of the strains isolated showed antagonistic effect against one or more entomopathogenic fungi, which could assist the beetle in its fight against this pathogenic threat. Using culture-dependent and -independent techniques, we present a taxonomical analysis of the bacteriome associated with theI. typographusbeetle during its different life stages. We have observed an evolution of its bacteriome, which is diverse at the larval phase, substantially diminished in pupae, greater in the teneral adult phase, and similar to that of the larval stage in mature adults. Our results suggest that taxa belonging to theErwiniaceaefamily, and thePseudoxanthomonasandPseudomonasgenera, as well as an undescribed genus within theEnterobactereaceaefamily, are part of the core microbiome and may perform vital roles in maintaining beetle fitness.ConclusionOur results indicate that isolates within the bacteriome ofI. typographusbeetle have the metabolic potential to increase beetle fitness by proving additional and assimilable carbon sources for the beetle, and by antagonizing fungi entomopathogens. Furthermore, we observed that isolates from adult beetles are more likely to have these capacities but those obtained from larvae showed strongest antifungal activity. Our taxonomical analysis showed thatErwinia typographi,Pseudomonas bohemica, andPseudomonas typographispecies along withPseudoxanthomonasgenus, and putative new taxa belonging to theErwiniaceaeandEnterobacteralesgroup are repeatedly present within the bacteriome ofI. typographusbeetles, indicating that these species might be part of the core microbiome. In addition toPseudomonasandErwiniagroup,Staphylococcus,Acinetobacter,Curtobacterium, Streptomyces, andBacillusgenera seem to also have interesting metabolic capacities but are present in a lower frequency. Future studies involving bacterial-insect interactions or analysing other potential roles would provide more insights into the bacteriome capacity to be beneficial to the beetle.Supplementary InformationThe online version contains supplementary material available at 10.1186/s40793-023-00510-z.