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Mal secco is a severe vascular citrus disease (MSD) caused by the mitosporic fungus <i>Plenodomus tracheiphilus</i> (<i>Pt</i>). The pathogen enters through wounds on the above- and below-ground parts of the tree. The susceptible species sour orange (<i>Citrus aurantium</i>) is the most commonly used rootstock for lemon trees in Italy. In this study, sour orange seedlings were wound-inoculated with <i>P. tracheiphilus</i> in leaves or roots. Six months post-inoculation, the microbial communities of rhizosphere, endorhizosphere, and xylem endosphere samples from inoculated and healthy plants were analyzed by 16S rRNA and ITS (internal transcribed spacer) amplicon sequencing. The DNA of <i>Pt</i> was quantified by real-time PCR in the three compartments. According to our results, the endorhizosphere of root-inoculated plants showed the highest concentration of the pathogen DNA. Bacterial populations of potentially beneficial taxa (e.g., <i>Pseudomonas</i> and <i>Burkholderia</i>) were depleted in the rhizosphere of the inoculated plants. Infection through leaves and roots also produced a network-wide rewiring of microbial associations in sour orange roots. Overall, our findings revealed community-level changes induced by <i>Pt</i> infection in the sour orange root and xylem microbiome, providing further insights into the beneficial multispecies interactions in <i>Citrus</i>-associated microbial communities.