Understanding the phyllomicrobiome dynamics in cauliflower plants holds significant promise for enhancing crop resilience against black rot disease, caused by Xanthomonas campestris pv. campestris. In this study, the culturable microbiome and metagenomic profile of tolerant (BR-161) and susceptible (Pusa Sharad) cauliflower genotypes were investigated to elucidate microbial interactions associated with disease tolerance. Isolation of phyllospheric bacteria from asymptomatic and black rot disease symptomatic leaves of tolerant and susceptible cultivars yielded 46 diverse bacterial isolates. Molecular identification via 16S rRNA sequencing revealed differences in the diversity of microbial taxa between genotypes and health conditions. Metagenomic profiling using next-generation sequencing elucidated distinct microbial communities, with higher diversity observed in black rot disease symptomatic leaf of BR-161. Alpha and beta diversity indices highlighted differences in microbial community structure and composition between genotypes and health conditions. Taxonomic analysis revealed a core microbiome consisting of genera such as Xanthomonas, Psychrobacillus, Lactobacillus, and Pseudomonas across all the samples. Validation through microbiological methods confirmed the presence of these key genera. The findings provide novel insights into the phyllomicrobiome of black rot-tolerant and susceptible genotypes of cauliflower. Harnessing beneficial microbial communities identified in this study offers promising avenues for developing sustainable strategies to manage black rot disease and enhance cauliflower crop health and productivity.