Background <p>Crop diversification through crop rotation or cover cropping is widely recognized as an important strategy to improve agroecosystem sustainability, enhance soil health, and suppress soilborne diseases. Rotating crops or introducing cover crops can disrupt pathogen life cycles, improve nutrient cycling, and promote beneficial microbes. However, the outcomes of diversification practices are often complex, influenced by soil type, crops, and pathogen pressures. Evaluating how cover crops and crop phase affect crop soilborne diseases and root-associated microbiome is critical for designing resilient cropping systems.</p> Results <p>This study evaluated the legacy effects of cover crops and crop phase on soybean root diseases and root-associated microbiome. Soybean plants were grown in soils collected from a corn-soybean rotation field experiment with and without cover crops, and then challenged with either <i>Fusarium graminearum</i> inoculum or soybean cyst nematode (SCN) in the growth chamber. Soils with a cover crop history significantly reduced <i>F. graminearum</i>-induced root rot, but had a limited impact on SCN, indicating divergent disease responses. Microbial profiling revealed that <i>F. graminearum</i> inoculum strongly reshaped bacterial communities, reducing Shannon diversity and enriching fast-growing copiotrophic taxa, including Bacteroidota genera (<i>Pedobacter</i>, <i>Chitinophaga</i>, <i>Flavobacterium</i>, and <i>Mucilaginibacter</i>) and Proteobacteria genera (<i>Dyella</i>, <i>Pseudomonas</i>, <i>Rhizobium</i>, and <i>Paraburkholderia</i>) regardless of cover crops. In contrast, SCN infection increased bacterial Shannon diversity in soybean-phase soils regardless of cover crops but decreased fungal Shannon diversity in soybean soils without cover crops, highlighting pathogen-specific microbial shifts. Cover cropping enhanced microbial heterogeneity under both pathogen pressures, enriching microbial taxa potentially involved in nutrient cycling (<i>Chitinophaga</i> and <i>Mucilaginibacter</i>), antagonism (<i>Flavobacterium</i>,<i> Streptomyces</i>, <i>Pseudonocardia</i>, and <i>Nocardioides</i>), and competitive interactions (<i>Paraburkholderia</i>). Correlation analyses further linked specific bacterial and fungal genera with disease suppression.</p> Conclusions <p>Soilborne pathogens and cropping practices exerted interconnected, pathogen- and crop-specific effects on root microbial communities. Cover cropping offers a promising strategy to enhance microbial-mediated disease resilience in soybean systems, providing ecological insights into microbiome-driven plant health.</p>