Plants interact with complex microbial communities in which microorganisms play different roles in plant development and health. While certain microorganisms may cause disease, others promote nutrient uptake and resistance to stresses through a variety of mechanisms. Developing plant protection measures requires a deeper comprehension of the factors that influence multitrophic interactions and the organization of phyllospheric communities. High-throughput sequencing was used in this work to investigate the effects of climate variables and bacterial wildfire disease on the bacterial community’s composition and assembly in the phyllosphere of tobacco (Nicotiana tabacum L.). The samples from June (M1), July (M2), August (M3), and September (M4) formed statistically separate clusters. The assembly of the whole bacterial population was mostly influenced by stochastic processes. PICRUSt2 predictions revealed genes enriched in the M3, a period when the plant wildfire disease index reached climax, were associated with the development of the wildfire disease (secretion of virulence factor), the enhanced metabolic capacity and environmental adaption. The M3 and M4 microbial communities have more intricate molecular ecological networks (MENs), bursting with interconnections within a densely networked bacterial population. The relative abundances of plant-beneficial and antagonistic microbes Clostridiales, Bacillales, Lactobacillales, and Sphingobacteriales, showed significant decrease in severally diseased sample (M3) compared to the pre-diseased samples (M1/M2). Following the results of MENs, we further test if the correlating bacterial pairs within the MEN have the possibility to share functional genes and we have unraveled 139 entries of such horizontal gene transfer (HGT) events, highlighting the significance of HGT in shaping the adaptive traits of plant-associated bacteria across the MENs, particularly in relation to host colonization and pathogenicity.