Quiescent bacteria are intrinsically resistant to antibiotics and the host immune response. A conserved bacterial starvation survival response is the consumption of ATP to make an inorganic polymer, polyphosphate (polyP), which then forms granule superstructures. PolyP granules occur in all three domains of life, yet how and why cells form these structures is poorly understood. Through high-resolution spatiotemporal characterization of de novo granule genesis, we find that polyP granule synthesis is required for and coordinated with cell cycle exit in the opportunistic pathogen Pseudomonas aeruginosa. PolyP has also been functionally connected with the cell cycle in eukaryotes, suggesting that polyP may be a broadly conserved mediator between metabolic state and the cell cycle.