Significance Cyclic electron flow around photosystem I (CEF) is critical for balancing the energy budget of photosynthesis, but its regulation is not well understood. Our results provide evidence that hydrogen peroxide, which is produced as a result of imbalances in chloroplast redox state, acts as a signaling agent to activate CEF in higher plants in vivo. Cyclic electron flow (CEF) around photosystem I is thought to balance the ATP/NADPH energy budget of photosynthesis, requiring that its rate be finely regulated. The mechanisms of this regulation are not well understood. We observed that mutants that exhibited constitutively high rates of CEF also showed elevated production of H ₂O ₂. We thus tested the hypothesis that CEF can be activated by H ₂O ₂ in vivo. CEF was strongly increased by H ₂O ₂ both by infiltration or in situ production by chloroplast-localized glycolate oxidase, implying that H ₂O ₂ can activate CEF either directly by redox modulation of key enzymes, or indirectly by affecting other photosynthetic processes. CEF appeared with a half time of about 20 min after exposure to H ₂O ₂, suggesting activation of previously expressed CEF-related machinery. H ₂O ₂-dependent CEF was not sensitive to antimycin A or loss of PGR5, indicating that increased CEF probably does not involve the PGR5-PGRL1 associated pathway. In contrast, the rise in CEF was not observed in a mutant deficient in the chloroplast NADPH:PQ reductase (NDH), supporting the involvement of this complex in CEF activated by H ₂O ₂. We propose that H ₂O ₂ is a missing link between environmental stress, metabolism, and redox regulation of CEF in higher plants.