Pathogens from the fastidious, phloem-restricted ‘Candidatus Liberibacter’ species cause the devastating Huanglongbing (HLB) disease in citrus worldwide and cause diseases on many solanaceous crops and plants in the Apiaceae family. However, little is known about the pathogenic mechanisms due to the difficulty in culturing the corresponding Liberibacters. Here we report that the citrus HLB pathogen ‘Ca. L. asiaticus’ (CLas) uses an active salicylate (SA) hydroxylase SahA to degrade SA and suppress plant defenses. Purified SahA protein displays strong enzymatic activity to degrade SA and its derivatives. Overexpression of SahA in transgenic tobacco plants abolishes SA accumulation and hypersensitive response (HR) induced by non-host pathogen infection. By degrading SA, CLas not only enhances the susceptibility of citrus plants to both nonpathogenic and pathogenic Xanthomonas citri (Xac), but also attenuates the responses of citrus plants to exogenous SA. In addition, foliar spraying of 2,1,3-benzothiadiazole (BTH) and 2,6-dichloroisonicotinic acid (INA), SA functional analogs not degradable by SahA, displays comparable (and even better) effectiveness with SA in suppressing CLas population growth and HLB disease progression in infected citrus trees under field conditions. This study demonstrates pathogen(s) suppresses plant defenses by degrading SA and establishes the clues for developing novel SA derivatives-based management approaches to control the associated plant diseases.