The photosystem II reaction centre protein D1 is encoded by the psbA gene. The D1 protein is stable in darkness but undergoes rapid turnover in the light. Here, we show that, in cyanobacterium Synechocystis sp. PCC6803, the synthesis of the D1 protein is regulated at the level of translation elongation in addition to the previously known transcriptional regulation. When Synechocystis sp. PCC6803 cells were transferred from light to darkness, the psbA mRNA remained abundant for hours. Cytosolic ribosomes were attached to psbA transcripts in the dark, and translation continued up to a distinct pausing site. However, ribosome nascent D1 chain complexes were not targeted to the thylakoid membrane, and no full-length D1 protein was produced in darkness. The arrest in translation elongation was released in the light, concomitantly with targeting of ribosome D1 nascent-chain complexes to the thylakoid membrane, allowing the synthesis of the full-length D1 protein. Downregulation of membrane targeting of ribosome complexes was also observed in the light if damage to the D1 protein was slow. This novel type of regulation of prokaryotic translation functions to balance the synthesis and degradation of the rapidly turning over photosystem II D1 protein in Synechocystis sp. PCC6803.