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<i>Popillia japonica</i> (<i>Coleoptera</i>: <i>Scarabaeidae</i>), is an emerging invasive pest in Europe and America. In the Azores, this pest was first found on Terceira Island during the sixties and soon spread to other islands. The rate of infestation differs between islands, and we hypothesized that microbiome composition could play a role. Therefore, we sampled 3rd instar larvae and soil from sites with high and low infestation rates to analyze the microbiome using next-generation sequencing. We analyzed twenty-four 16S DNA libraries, which resulted in 3278 operational taxonomic units. The alpha and beta diversity of the soil microbiome was similar between sites. In contrast, the larvae from high-density sites presented a higher bacterial gut diversity than larvae from low-density sites, with biomarkers linked to plant digestion, nutrient acquisition, and detoxification. Consequently, larvae from high-density sites displayed several enriched molecular functions associated with the families <i>Ruminococcaceae</i>, <i>Clostridiaceae</i> and <i>Rikenellaceae</i>. These bacteria revealed a supportive function by producing several CAZyme families and other proteins. These findings suggest that the microbiome must be one drive for the increase in <i>P. japonica</i> populations, thus providing a checkpoint in the establishment and spread of this pest.