Aphids are small insects that have developed specialized mouthparts and effector proteins to establish long-term relationships with plants. The peach-potato aphid is a generalist, feeding on many plant species and capable of transmitting numerous pathogens. This study reveals how host-responsive cathepsin B (CathB) proteins in the oral secretions of facilitate aphid survival by modulating plant immune responses. Host-responsive CathB proteins localize to plant processing bodies (p-bodies), cytoplasmic ribonucleoprotein granules involved in messenger RNA storage or decay. Upon localization, these CathB proteins recruit key immune regulators EDS1, PAD4, and ADR1 to these bodies, suppressing plant defenses. A plant protein, Acd28.9 (Hsp20 family), counteracts this CathB activity and contributes to plant resistance to aphids. These findings highlight an unexpected role for p-bodies in plant immunity and uncover a plant resistance mechanism to aphid infestation.