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Verticillium wilt caused by <i>Verticillium</i> spp. results in severe yield losses in a broad range of crops. <i>Verticillium</i> outbreaks are challenging to control, and exacerbated by increases in soil temperatures and drought associated with global warming. Employing natural antagonists as biocontrol agents offers a promising approach to addressing this challenge. <i>Paenibacillus polymyxa</i> Sb3-1 was proven to reduce the growth of <i>Verticillium longisporum</i> during <i>in vitro</i> experiments and was shown to promote the growth of oilseed rape seedlings infested with <i>V. longisporum</i>. Our novel approach combined <i>in vitro</i> and <i>in planta</i> methods with the study of the mode of interaction between Sb3-1 and <i>V. longisporum</i> EVL43 via their volatile organic compounds (VOCs). Volatile and soluble substances, produced by both microorganisms as a reaction to one another's VOCs, were detected by using both gas and liquid chromatography-mass spectrometry. <i>P. polymyxa</i> Sb3-1 continually produced antimicrobial and plant growth promoting VOCs, such as 2-nonanone and 3-hydroxy-2-butanone. Several other antimicrobial volatile substances, such as isoamyl acetate and durenol, were downregulated. The general metabolic activity of Sb3-1, including protein and DNA biotransformations, was upregulated upon contact with EVL43 VOCs. <i>V. longisporum</i> increased its production of antimicrobial substances, such as 1-butanol, and downregulated its metabolic activities upon exposure to Sb3-1 VOCs. Additionally, several stress response substances such as arabitol and protein breakdown products (e.g., L-Isoleucyl-L-glutamic acid), were increased in the co-incubated samples. The results obtained depict an ongoing dialog between these microorganisms resulting in growth inhibition, the slowing down of metabolism, and the cell death of <i>V. longisporum</i> due to contact with the <i>P. polymyxa</i> Sb3-1 VOCs. Moreover, the results indicate that VOCs make a substantial contribution to the interaction between pathogens and their natural antagonists and have the potential to control pathogens in a novel, environmentally friendly manner.