In a process termed quorum sensing (QS), the opportunistic bacterial pathogen Pseudomonas aeruginosa uses diffusible signaling molecules to regulate the expression of numerous secreted factors or public goods that are shared within the population. But not all cells respond to QS signals. These social cheaters typically harbor a mutation in the QS receptor gene lasR and exploit the public goods produced by cooperators. Here we show that non-social adaptation under growth conditions that require QS-dependent public goods increases tolerance to cheating and defers a tragedy of the commons. The underlying mutation is in the transcriptional repressor gene psdR. This mutation has no effect on public goods expression but instead increases individual fitness by derepressing growth-limiting intracellular metabolism. Even though psdR mutant populations remain susceptible to invasion by isogenic psdR lasR cheaters, they bear a lower cheater load than do wild-type populations, and they are completely resistant to invasion by lasR cheaters with functional psdR. Mutations in psdR also sustain growth near wild-type levels when paired with certain partial loss-of-function lasR mutations. Targeted sequencing of multiple evolved isolates revealed that mutations in psdR arise before mutations in lasR, and rapidly sweep through the population. Our results indicate that a QS-favoring environment can lead to adaptations in non-social, intracellular traits that increase the fitness of cooperating individuals and thereby contribute to population-wide maintenance of QS and associated cooperative behaviors.