The type III secretion system (T3SS) is a well-characterized virulence apparatus in pathogenic bacteria, yet its role in beneficial rhizobacteria has remained largely elusive. Using the plant growth-promoting rhizobacteria (PGPR) Pseudomonas fluorescens 2P24 as a model, this study systematically deciphered the secretome of its T3SS. We demonstrate that T3SS in PGPR promotes the secretion of a niche-constructing enzymatic toolkit while actively suppressing the release of proteins conducive to a free-living state. Thus, this work redefines a classic virulence apparatus in mutualism and provides a mechanistic framework for engineering beneficial plant-microbe interactions.