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Abstract Cyanobacteria contribute to roughly a quarter of global net carbon fixation. During diel light/dark growth, dark respiration substantially lowers the overall photosynthetic carbon yield in cyanobacteria and other phototrophs. How respiratory pathways participate in carbon resource allocation at night to optimize dark survival and support daytime photosynthesis remains unclear. Here, using the cyanobacterium Synechococcus elongatus PCC 7942, we show that phosphoketolase integrates into a respiratory network in the dark to best allocate carbon resources for amino acid biosynthesis and to prepare for photosynthesis reinitiation upon photoinduction. Moreover, we show that the respiratory Entner–Doudoroff pathway in S. elongatus is incomplete, with its key enzyme 2-keto-3-deoxy-6-phosphogluconate aldolase exhibiting alternative oxaloacetate decarboxylation activity that modulates daytime photosynthesis. This activity allows for the bypassing of the tricarboxylic acid cycle when ATP and NADPH consumption for biosynthesis is excessive and imbalanced relative to their production by the light reactions, thereby preventing relative NADPH accumulation and ensuring optimal photosynthetic carbon yield. Optimizing these metabolic processes offers opportunities to enhance photosynthetic carbon yield in cyanobacteria and other photosynthetic organisms under diel light/dark cycles.