Tomato bacterial canker caused byClavibacter michiganensis(Cm) is considered to be one of the most destructive bacterial diseases of tomato. To date, no resistance to the pathogen has been identified. While several molecular studies have identified (Cm) bacterial factors involved in disease development, the plant genes and mechanisms associated with susceptibility of tomato to the bacterium remain largely unknown. Here, we show for the first time that tomato geneSlWAT1is a susceptibility gene toCm. We inactivated the geneSlWAT1through RNAi and CRISPR/Cas9 to study changes in tomato susceptibility toCm. Furthermore, we analysed the role of the gene in the molecular interaction with the pathogen. Our findings demonstrate thatSlWAT1functions as an S gene to genetically diverseCmstrains. Inactivation ofSlWAT1reduced free auxin contents and ethylene synthesis in tomato stems and suppressed the expression of specific bacterial virulence factors. However, CRISPR/Cas9slwat1mutants exhibited severe growth defects. The observed reduced susceptibility is possibly a result of downregulation of bacterial virulence factors and reduced auxin contents in transgenic plants. This shows that inactivation of an S gene may affect the expression of bacterial virulence factors.