Aims <p>This study investigated how infection by the invasive pathogen <i>Cronartium ribicola</i> (pine blister rust) restructures the multicompartment of <i>Pinus armandii</i>, encompassing the needle, bark, root, and rhizosphere soil. To reveal the underlying mechanisms, we explored the relationships between changes in microbial network topology and community structure and disease onset, offering an ecological insight into disease etiology.</p> Methods <p>Microbial communities in four host niches were characterized and compared between healthy and infected <i>P. armandii</i> trees. We applied amplicon sequencing combined with co-occurrence network analysis to assess changes in network topology, including complexity, modularity, and stability. Random forest modeling was used to identify key predictors of disease occurrence among microbial diversity indices, network topological properties, and soil physicochemical parameters.</p> Results <p>Infection altered fungal and bacterial community diversity and reshaped microbial networks in a niche-specific manner. Community composition varied across host niches, with the rhizosphere soil being the only exception. Network analysis indicated that root-associated microbial networks became more topologically complex but less stable. By contrast, networks in bark exhibited improved modularity and robustness. Random forest modeling demonstrated that changes in bark microbial network properties were the primary predictors of disease occurrence, accounting for 37.1% of the total variance.</p> Conclusions <p>The progression of pine blister rust extends beyond direct pathogenicity, driving ecological dysbiosis via destabilized root microbiomes and topological degradation of bark networks. These findings highlight the role of the host's extended ecological network in disease development. Targeting microbial resilience at key plant-soil interfaces, particularly the bark and root, may offer a practical approach for maintaining the health of <i>P. armandii</i>.</p>