Tomato is a strategic crop grown in Egypt with unfortunate sensitivity to wilt diseases causing tons and millions of losses. Plant Growth-Promoting Rhizobacteria (PGPR) is a suitable bioagent to activate systemic resistance, improve plant health, and replace expensive chemical pesticides. Therefore, the current study investigated the potential antagonistic activity of four PGPR strains [Pseudomonas alcaligenes (denoted as YMB9), Bacillus subtilis (YMB8), Pseudomonas indica (YMB4), and Bacillus licheniformis (YMB3)] against two tomato wilt causing pathogens [Fusarium oxysporum and Ralstonia solanacearum]. Abilities to produce inhibitory metabolites [Siderophores and Hydrogen Cyanide (HCN)], plant growth hormones [Indole-3-Acetic Acid (IAA)] and solubilize soil phosphate were approved by molecular and microbiological approaches to all four strains. After 24- and 48-hours post-infection, significant changes at the level of gene expression were revealed using the semi-quantitative real-time PCR associated with the three-tomato hormonal, signaling, and defense mechanisms. Compared to the untreated plants, the YMB9 strain has differentially modulated the three genes [pathogenesis-related protein 1 (pr.1a; p≤0.05), protease inhibitor II (pin2; p≤0.001), and osmotin-like (osm; p≤0.001)] as indicators to the three signaling pathways of salicylic and jasmonic acids and ethylene; respectively. Supportively, the scanning electron microscopy revealed robust adherence of the rhizobacterial cells to the tomato roots causing the activation of tomato systemic resistance against the two tomato wilt pathogens. This proves the bioagent role of rhizobacteria in enhancing crop resilience and clean sustainable agriculture.