In a process called quorum sensing (QS), the bacterial pathogen Pseudomonas aeruginosa uses small diffusible signals to coordinate cooperative behaviors via secreted “public goods”. Under QS-dependent growth conditions, social cheaters arise with mutations in lasR, the gene for the primary QS signal receptor. These cheaters do not produce public goods. They impart a burden on the cooperators in the population that can lead to a tragedy of the commons in which the population collapses. During in vitro evolution on casein medium that requires QS-dependent protease secretion, a non-social adaptation occurs early in the transcriptional repressor gene psdR that increases peptide uptake, allowing toleration of a greater cheater load and delaying population collapse. In this study, we use whole genome sequencing to identify mutations that arise late in experimental evolution. We characterize prevalent loss-of-function mutations in the alternative sigma factor gene rpoS. These mutants display normal QS abilities in non-cooperative growth conditions, but are unable to grow in single culture on casein. rpoS mutants show increased fitness when grown in co-culture with the wild-type. Previous microarray data show that RpoS represses the same set of peptide uptake genes as PsdR and induces a secreted aminopeptidase, PaAP, providing a possible mechanism. Overall, our results suggest that inactivation of rpoS results in both cooperative and non-cooperative adaptations in P. aeruginosa, contributing to our understanding of processes that shape cooperative behavior in bacteria.