Summary In plants, rubisco activase (Rca) regulates rubisco by removing inhibitory molecules such as ribulose‐1,5‐bisphosphate (RuBP). In cyanobacteria, a homologous protein (activase‐like cyanobacterial protein, ALC), contains a distinctive C‐terminal fusion resembling the small‐subunit of rubisco. Although cyanobacterial rubisco is believed to be less sensitive to RuBP inhibition, the ALC is widely distributed among diverse cyanobacteria. Using microscopy, biochemistry and molecular biology, the cellular localization of the ALC, its effect on carboxysome/cell ultrastructure in Fremyella diplosiphon, and its function in vitro were studied. Bioinformatic analysis uncovered evolutionary relationships between the ALC and rubisco. ALC localizes to carboxysomes and exhibits ATPase activity. Furthermore, the ALC induces rubisco aggregation in a manner similar to that of another carboxysomal protein, M35, and this activity is affected by ATP. An alc deletion mutant showed modified cell morphology when grown under enriched CO2 and impaired regulation of carboxysome biogenesis, without affecting growth rate. Carbamylation of Fremyella recombinant rubisco was inhibited by RuBP, but this inhibition was not relieved by the ALC. The ALC does not appear to function like a canonical Rca; instead, it exerts an effect on the response to CO2 availability at the level of a metabolic module, the carboxysome, through rubisco network formation, and carboxysome organization.