Pseudomonas aeruginosa PA14, an opportunistic pathogen of diverse hosts, contains genes with the potential to confer production of R-bodies (i.e., a “reb cluster”). R-bodies are large, extendable protein polymers best known for their role in killing of paramecia by the bacterium Caedibacter taeniospiralis, and genes in the reb cluster have been implicated in PA14 virulence. Here, we present evidence that PA14 expresses reb cluster genes during colonization of plant and nematode hosts. We identify products of the reb cluster that are R-body-associated and that control stochastic expression of R-body structural genes. We also show that R-body production is required for full virulence in nematodes. Analyses of nematode ribosome content and immune response indicate that R-bodies act via a mechanism involving ribosome cleavage and translational inhibition. These observations provide insight into the biology of R-body production and its consequences during P. aeruginosa infection