Coupling cell cycle with nutrient availability is a crucial process for all living cells. But how bacteria control cell division according to metabolic supplies remains poorly understood. Here, we describe a molecular mechanism that coordinates central metabolism with cell division in the α-proteobacterium Caulobacter crescentus. This mechanism involves the NAD-dependent glutamate dehydrogenase GdhZ and the oxidoreductase-like KidO. While enzymatically active GdhZ directly interferes with FtsZ polymerization by stimulating its GTPase activity, KidO bound to NADH destabilizes lateral interactions between FtsZ protofilaments. Both GdhZ and KidO share the same regulatory network to concomitantly stimulate the rapid disassembly of the Z-ring, necessary for the subsequent release of progeny cells. Thus, this mechanism illustrates how proteins initially dedicated to metabolism coordinate cell cycle progression with nutrient availability. Synopsis GdhZ and KidO are metabolic regulators of cell division in Caulobacter crescentus. Once bound to their substrates, both proteins synergistically stimulate cytokinesis by triggering Z-ring disassembly by two complementary mechanisms in late predivisional cells (G2). Caulobacter crescentus modulates cell division according to its metabolic activity. Catalytically active GdhZ stimulates GTPase activity of FtsZ. KidO bound to NADH inhibits lateral interactions between FtsZ protofilaments. KidO and GdhZ cooperate to disassemble the Z-ring. GdhZ and KidO are complementary negative regulators of FtsZ that connect metabolic conditions to cell division in Caulobacter crescentus. GdhZ is an inhibitor of FtsZ polymerization while KidO prevents FtsZ filament bundling in response to nutrient availability.