Bacteria sense population density via the cell-cell communication system called quorum sensing (QS). In closed environments, nutrients are depleted as biomass increases, which eventually restricts cell growth and alters non-essential bacterial behaviors. We uncovered a phenomenon in which Vibrio cells optimize expression of the methionine and tetrahydrofolate (THF) synthesis genes via QS as population density changes. 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 de-repressed by LuxR at high cell density as glucose becomes limiting. In mixed cultures, QS mutant strains (cheaters) can initially co-exist with wildtype strains, but as glucose is depleted, wild-type strains outcompete the cheaters. Thus, coupling of methionine synthesis to QS regulation de-incentivizes evolution of cheater cells.