Significance The evolution of photosynthetic cyanobacteria under 24-h cycles of light and darkness selected for a robust circadian clock. Understanding how cyanobacteria integrate circadian clock signals with natural light–dark cycles to control metabolism is critical, because these organisms are central to global carbon cycling and hold promise for development of renewable energy. Here we assess how the circadian transcription factor regulator of phycobilisome association A (RpaA) influences metabolism as a cyanobacterium goes through a light-to-dark transition. The data show that RpaA plays a key role in maintaining metabolic stability during the night period. Additionally, RpaA is important in controlling redox balance, which in turn is very important for regulating metabolism at night.