Ips typographus, the most serious pest of spruce forests in Europe, is associated with microorganisms facilitating its invasion and development inside spruce tissues. Despite the importance of I. typographus, little is known about its core gut microbiome. Hereby, we describe the composition of bacterial and fungal microbiomes throughout I. typographus life cycle in spring and summer generations. We used cultivation technique and molecular identification in combination with DNA and RNA metabarcoding to achieve deep inside into the beetle’s microbiome composition and structure. As it is not known whether microbiome forms stable communities inside the beetle’s gut, we observed gut epithelium for biofilm formation with Transmission Electron Microscopy. Cultivation technique together with DNA and RNA metabarcoding indicated similar dominant taxa. The bacterial community belongs almost exclusively to the phylum Proteobacteria (newly Pseudomonadota) and the most common orders and genera are Enterobacteriales (Erwinia and Serratia), Pseudomonadales (Pseudomonas) and Xanthomonadales (Pseudoxanthomonas, Stenotrophomonas). Yeasts (Saccharomycetes) highly dominated the fungal microbiome, followed by Sordariomycetes represented mainly by Ophiostoma bicolor and Endoconidiophora polonica. The most common yeasts were Wickerhamomyces bisporus, Kuraishia molischiana, Nakazawaea ambrosiae, Yamadazyma spp. and Cyberlindnera sp. The proportions of the dominant taxa belonging to the core microbiome of I. typographus change throughout its life cycle and generations. We did not observe any biofilm formation on gut epithelium, which suggests that microbial cells pass through the beetle’s gut with chyme. We propose that species belonging to the core microbiome has similar functions and alternate in the I. typographus ecosystem depending on environmental conditions.