<p>Bacterial diseases are a major and growing threat to crop production around the world. Antimicrobial resistance, regulatory restrictions, and environmental concerns are making it harder for traditional bactericides to control bacterial plant pathogens (BPPs). Bacteriophages have reemerged as promising biocontrol agents (BCAs) due to their host specificity, self-amplifying nature, and environmental safety. However, most phage-based biocontrol strategies have been developed within a single-pathogen framework, overlooking the complex microbial communities that govern pathogen establishment, persistence, and disease outcomes. Recent advances in microbiome research reveal that plant health is strongly influenced by phage-microbiome interactions within the phyllosphere and rhizosphere, positioning bacteriophages as ecological modulators rather than merely antibacterial tools. This review synthesizes current knowledge on the diversity, ecology, and functional roles of bacteriophages in plant-associated microbiomes and critically examines how phage application reshapes microbial community structure, promotes microbiome resilience, and indirectly enhances disease suppression by modulating plant immune responses. In addition, we evaluate technological advances including viromics, multi-omics integration, and synthetic community models that are transforming our ability to study phage-microbiome dynamics in agricultural systems. Key challenges that may interfere with phage-based biocontrol strategies are environmental stability, phage resistance, biosafety, and regulatory frameworks are also addressed. By integrating ecological theory with applied biocontrol research, this review proposes a roadmap for the development of next-generation phage-based strategies that are robust, sustainable, and adaptable to climate driven changes in agroecosystems.</p>