Anthracnose threatens sorghum productivity globally, with yield losses exceeding 50 % in some cases, making it crucial to understand plant-microbe-pathogen interactions to develop effective, sustainable control strategies. To probe deeper into the complexity of plant-microbe-pathogen relationships, this study used high-throughput sequencing to characterize microbial communities present in association with sorghum leaves and seeds harvested from both anthracnose infected and uninfected control plants. Our analysis shows that the variation in the diversity and composition of the microbiome due to anthracnose is indicative of an adaptive regulation by coexisting microbes with a plant for enhancing resistance against stresses. These changes were not only reflected by community composition, but also had remarkable effects on the topological properties of microbial ecological networks which further influence certain functions as well as key functional guilds related to plant growth. The presence of anthracnose significantly increased network complexity and resistance in the phyllosphere and leaf endosphere meta-microbiome, which may reflect an adaptive microbiome response to pathogen. The seed-associated microbiomes, however, had relatively no change in diversity and network properties indicating a stable background that may repel pathogen invasion. The study also suggests that anthracnose may facilitate its spread through the reorganization of microbial communities and the enrichment of specific beneficial microbes, aiding in plant defense against pathogens. This is achieved through an upregulation of siderophore production, antimicrobial compounds, phosphate solubilization and sulfur metabolism-specifically genes. Our work also uncovers the possibility for microbiome transfer through phyllosphere-and seed associated microbiomes, thereby indicating that pathogen spread between both above and below ground plant niches limit management options. To conclude, the present study reveals fresh insights into how plant-associated microbiomes respond to anthracnose stress and offers insight on their prospective in sustainable agriculture.