The remarkably stable circadian oscillations of single cyanobacteria enable a population of growing cells to maintain synchrony for weeks in constant environmental conditions. These oscillations are generated by a network architecture that consists of two regulatory loops: (i) a posttranslational regulation (PTR) circuit and (ii) a transcriptional-translational feedback regulation (TTR) circuit. We addressed the question of the utility of two circuits. We found that the PTR circuit is sufficient to generate oscillations in growing cyanobacteria. However, in the absence of TTR, individual oscillators were less stable and synchrony was not maintained in a population of cells. Experimentally constrained mathematical modeling reproduced sustained oscillations in the PTR circuit alone and demonstrated the importance of TTR for oscillator synchrony.