AbstractBACKGROUNDPhenacoccus solenopsis is a polyphagous invasive mealybug that caused serious damage to crops worldwide. Phloem‐sucking hemipterans are known to carry symbiotic microbes in their saliva. However, the role of salivary bacteria of P. solenopsis in modulating plant defenses remains limited. Exploring the impact of salivary bacteria on plant defense responses will contribute to the development of new targets for efficient control of invasive mealybugs.RESULTSSalivary bacteria of the invasive mealybug P. solenopsis can suppress herbivore‐induced plant defenses and thus enhance mealybug fitness. Mealybugs treated with an antibiotic showed decreased weight gain, fecundity and survival. Untreated mealybugs suppressed jasmonic acid (JA)‐regulated defenses but activated salicylic acid (SA)‐regulated defenses in cotton plants. In contrast, antibiotic‐treated mealybugs triggered JA‐responsive gene expression and JA accumulation, and showed shortened phloem ingestion. Reinoculating antibiotic‐treated mealybugs with Enterobacteriaceae or Stenotrophomonas cultivated from mealybug saliva promoted phloem ingestion and fecundity, and restored the ability of mealybugs to suppress plant defenses. Fluorescence in situ hybridization visualization revealed that Enterobacteriaceae and Stenotrophomonas colonize salivary glands and are secreted into the mesophyll cells and phloem vessels. Exogenous application of the bacterial isolates to plant leaves inhibited JA‐responsive gene expression and activated SA‐responsive gene expression.CONCLUSIONOur findings imply that symbiotic bacteria in the saliva of the mealybug play an important role in manipulating herbivore‐induced plant defenses, enabling this important pest to evade induced plant defenses and promoting its performance and destructive effects on crops. © 2023 Society of Chemical Industry.