Updated publication reference for PubMed record(s): 31740681. Clonal bacterial populations respond to unfavorable conditions with growth arrest and 20 persistence. Here we show that quorum sensing (QS) determines functionally distinct subpopulations of non-growing, virulent Legionella. QS increases the fraction of bacteria re- initiating growth in microcolonies, while it restricts the ratio of bacteria resuming growth in free- living protozoan predators. QS continues to govern the population heterogeneity throughout growth. Intracellular non-growers and growing bacteria are characterized by distinct proteomes 25 reflecting different stress and drug tolerance as well as alternative metabolic pathways. Strikingly, individual intracellular non-growers are persisters, which endure host killing mechanisms, produce virulence factors, form a replication-permissive compartment, and are highly infectious. Thus, QS underlies a bet-hedging strategy of non-growing intracellular bacterial pathogens to resume growth and to fine-tune virulence.