The supramolecular organization of membrane proteins (MPs) is sensitive to environmental changes in photosynthetic organisms. Isolation of MP supercomplexes from the green algae Chlamydomonas reinhardtii, which are believed to contribute to cyclic electron flow (CEF) between the cytochrome b6f complex (Cyt-b6f) and photosystem I (PSI), proved difficult. We were unable to isolate a supercomplex containing both Cyt-b6f and PSI because in our hands, most of Cyt-b6f did not comigrate in sucrose density gradients, even upon using chemical cross-linkers or amphipol substitution of detergents. Assisted by independent affinity purification and MS approaches, we utilized disintegrating MP assemblies and demonstrated that the algae-specific CEF effector proteins PETO and ANR1 are bona fide Cyt-b6f interactors, with ANR1 requiring the presence of an additional, presently unknown, protein. We narrowed down the Cyt-b6f interface, where PETO is loosely attached to cytochrome f and to a stromal region of subunit IV, which also contains phosphorylation sites for the STT7 kinase.