The fire blight pathogen Erwinia amylovora requires a functional type III secretion system (T3SS) and the production of the exopolysaccharide amylovoran to cause disease. The GacS/GacA two-component system is widely conserved among gammaproteobacteria and is a global regulator of virulence factors. This system positively regulates non-coding small regulatory RNA csrB, which in turn binds to CsrA, a translational regulator. In this study, we characterized the grrA, csrB and csrA mutants. Results showed that the grrA and csrB mutants had similar phenotypes: both were hypermotile, produced a higher amount of amylovoran, and had increased expression of T3SS genes in vivo. In contrast, the csrA mutant exhibited the opposite phenotypes, including non-motility, no amylovoran production and no expression of T3SS genes. Furthermore, the csrA mutant did not induce hypersensitive response on non-host tobacco plants neither caused disease on immature pear fruit and apple shoots, indicating that CsrA is a positive regulator of virulence factors. These findings suggest that negative regulation of virulence by GrrS/GrrA acts through csrB, which likely binds to CsrA, antagonizing its positive effect on T3SS gene expression, flagellar formation and amylovoran production.