Summary Cyanobacteria perform water‐splitting photosynthesis and are important primary producers impacting the carbon and nitrogen cycles at global scale. They fix CO 2 through ribulose‐bisphosphate carboxylase/oxygenase ( RuBisCo ) and have evolved a distinct CO 2 concentrating mechanism ( CCM ) that builds high CO 2 concentrations in the vicinity of RuBisCo favouring its carboxylase activity. Filamentous cyanobacteria such as A nabaena fix CO 2 in photosynthetic vegetative cells, which donate photosynthate to heterocysts that rely on a heterotrophic metabolism to fix N 2 . CCM elements are induced in response to inorganic carbon limitation, a cue that exposes the photosynthetic apparatus to photodamage by over‐reduction. An A nabaena mutant lacking the LysR ‐type transcription factor A ll3953 grew poorly and dies under high light. The rbcL operon encoding RuBisCo was induced upon carbon limitation in the wild type but not in the mutant. ChIP ‐ S eq analysis was used to globally identify A ll3953 targets under carbon limitation. Targets include, besides rbcL , genes encoding CCM elements, photorespiratory pathway‐ photosystem‐ and electron transport‐related components, and factors, including flavodiiron proteins, with a demonstrated or putative function in photoprotection. Quantitative reverse transcription polymerase chain reaction analysis of selected A ll3953 targets showed regulation in the wild type but not in the mutant. A ll3953 ( PacR ) is a global regulator of carbon assimilation in an oxygenic photoautotroph.