Many insects form mutualistic relationships with microbial symbionts, crucial for their physiological processes. The bean bug, Riptortus pedestris, establishes a unique gut symbiosis with the genus Caballeronia and consistently acquires these symbionts from surrounding soil with each generation. As a result, the bean bug unavoidably consumes a variety of environmental microbes, including potential pathogens. To address this, the bean bug has developed a specialized organ in its midgut that selectively filters out non-symbiotic microbes, thereby preventing contamination of its symbiotic organ. In this study, we identified a pathogenic strain from the genus Burkholderia that lethally affects the bean bug post-invasion of the symbiotic organ. This pathogen employs a strategy of mimicking the motility of native symbionts to infiltrate the symbiont sorting organ and displays a pronounced resistance against antimicrobial agents produced by the host. Upon establishing itself in the symbiotic organ, the pathogen breaches the midgut cells, leading to host mortality, and subsequently disperses into the external environment. Our findings unveil a cunning pathogenic tactic that exploits the mimicry of native symbionts within an insect's symbiotic framework.