<p>Peanut (<i>Arachis hypogaea</i> L.) roots sustain complex chemical dialogues with their microbiome. These interactions are essential because exudate-mediated signaling governs microbial recruitment, cooperation, and stress resilience, yet the underlying regulatory grammars remain poorly understood. This review aims to elucidate how peanut root exudates orchestrate microbial assembly and function, identify regulatory feedback mechanisms, and highlight translational strategies for crop resilience. Emerging evidence indicates that peanut roots utilize a dual-circuit secretome: a constitutive lipid-rich baseline scaffolds microbial communities, while a stimulus-responsive stream of peptides, phenolics, sugars, and volatile organic compounds fine-tunes microbial behavior. Specialized metabolites including lipid-conjugated stilbenoids, sulfurated VOCs, and degradation-resistant lactone analogs serve as high-information ligands coordinating beneficial microbes and suppressing pathogens. Additional signaling pathways likely involve sORF- and lncRNA-derived micropeptides, extracellular vesicles carrying quorum-quenching cargo, and phase-separated receptor microdomains enhancing signal integration. A tri-timescale regulatory architecture, rapid ion-flux valves, intermediate post-translational modifications, and long-term epigenomic memory closes exudate–microbe–gene feedback loops, enabling stress adaptation and community-level resilience. Despite these advances, major knowledge gaps persist in spatiotemporal signaling and causal feedbacks. Thus, addressing these requires nano-scale spatial omics, closed-loop discovery systems, dual-species genetics, and rhizosphere conditional-essentiality mapping. Moreover, translational strategies such as Directed Exudation Engineering, synthetic communities with safety-by-design circuitry, precision VOC irrigation, and host-guided quorum quenching can enable durable, field-relevant microbiome engineering.</p>