Introduction Plant–microbiome interactions in the rhizosphere are critical for plant adaptation to environmental stress; however, the coordinated roles of root exudates and microbiome dynamics remain poorly understood. Methods Integrating untargeted metabolomics and shotgun metagenomics, we analyzed drought responses in drought-tolerant and drought-sensitive bermudagrass genotypes. Results Drought stress shaped the root exudate chemistry, which likely reprogrammed microbiome functions, such as TccC toxins and the Type VI secretion system, without considerable broad taxonomic shifts. A few metabolites, including riboflavin and 1-carboxy-6-hydroxy-3,4-dihydro-beta-carboline, were associated with Massilia putida , particularly in the rhizosphere of the drought-tolerant genotype. Discussion Our data suggest a potential explanation for a genotype-driven strategy of microbiome modulation via metabolite signaling.