Bacteria sense population density via the cell-cell communication system called quorum sensing (QS). Some QS-regulated phenotypes ( e.g. , secreted enzymes, chelators), are public goods exploitable by cells that stop producing them. We uncovered a phenomenon in which Vibrio cells optimize expression of the methionine and tetrahydrofolate (THF) synthesis genes via QS. Strains that are genetically 'locked' at high cell density grow slowly in minimal glucose media and suppressor mutants accumulate via inactivating-mutations in metF (methylenetetrahydrofolate reductase) and luxR (the master QS transcriptional regulator). Methionine/THF synthesis genes are repressed at low cell density when glucose is plentiful and are de-repressed by LuxR at high cell density as glucose becomes limiting. In mixed cultures, QS mutant strains initially co-exist with wild-type, but as glucose is depleted, wild-type outcompetes the QS mutants. Thus, QS regulation of methionine/THF synthesis is a fitness benefit that links private and public goods within the QS regulon, preventing accumulation of QS-defective mutants.