| Summary: | <i>Philaenus spumarius</i> (Linnaeus, 1758) (Hemiptera, Aphrophoridae) was recently classified as a pest due to its ability to act as a vector of the phytopathogen <i>Xylella fastidiosa</i>. This insect has been reported to harbour several symbiotic bacteria that play essential roles in <i>P. spumarius</i> health and fitness. However, the factors driving bacterial assemblages remain largely unexplored. Here, the bacteriome associated with different organs (head, abdomen, and genitalia) of males and females of <i>P. spumarius</i> was characterized using culturally dependent and independent methods and compared in terms of diversity and composition. The bacteriome of <i>P. spumarius</i> is enriched in Proteobacteria, Bacteroidota, and Actinobacteria phyla, as well as in <i>Candidatus</i> Sulcia and <i>Cutibacterium</i> genera. The most frequent isolates were <i>Curtobacterium</i>, <i>Pseudomonas</i>, and <i>Rhizobiaceae</i> sp.1. Males display a more diverse bacterial community than females, but no differences in diversity were found in distinct organs. However, the organ shapes the bacteriome structure more than sex, with the Microbacteriaceae family revealing a high level of organ specificity and the Blattabacteriaceae family showing a high level of sex specificity. Several symbiotic bacterial genera were identified in <i>P. spumarius</i> for the first time, including <i>Rhodococcus</i>, <i>Citrobacter</i>, <i>Halomonas</i>, <i>Streptomyces</i>, and <i>Providencia</i>. Differences in the bacterial composition within <i>P. spumarius</i> organs and sexes suggest an adaptation of bacteria to particular insect tissues, potentially shaped by their significance in the life and overall fitness of <i>P. spumarius</i>. Although more research on the bacteria of <i>P. spumarius</i> interactions is needed, such knowledge could help to develop specific bacterial-based insect management strategies.
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