The rhizosphere is a thin film of soil that surrounds plant roots and the primary location of nutrient uptake, and is where important physiological, chemical, and biological activities are occurring. Many microbes invade the rhizosphere and have the capacity to promote plant growth and health. Bacillus spp. is the most prominent plant growth promoting rhizobacteria due to its ability to form long-lived, stress-tolerant spores. Bacillus-plant interactions are driven by chemical languages constructed by a wide spectrum of metabolites and lead to enhanced plant growth and defenses. Thus, this review is a synthesis and a critical assessment of the current literature on the application of Bacillus spp. in agriculture, highlighting gaps that remain to be explored to improve and expand on the Bacillus-based biostimulants. Furthermore, we suggest that omics sciences, with a focus on metabolomics, offer unique opportunities to illuminate the chemical intercommunications between Bacillus and plants, to elucidate biochemical and molecular details on modes of action of Bacillus-based formulations, to generate more actionable insights on cellular and molecular events that explain the Bacillus-induced growth promotion and stress resilience in plants.