The inheritance of memory is an adaptive trait. Microbes challenge the immunity of organisms and trigger behavioral adaptations that can be inherited, but how bacteria produce inheritance of a trait is unknown. We use and its bacteria to study the transgenerational RNA dynamics of interspecies crosstalk leading to a heritable behavior. A heritable response of to microbes is the pathogen-induced diapause (PIDF), a state of suspended animation to evade infection. We identify RsmY, a small RNA involved in quorum sensing in as a trigger of PIDF. The histone methyltransferase (HMT) SET-18/SMYD3 and the argonaute HRDE-1, which promotes multi-generational silencing in the germline, are also needed for PIDF initiation The HMT SET-25/EHMT2 is necessary for memory maintenance in the transgenerational lineage. Our work is a starting point to understanding microbiome-induced inheritance of acquired traits, and the transgenerational influence of microbes in health and disease.