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The GreenCut encompasses a suite of nucleus‐encoded proteins with orthologs among green lineage organisms (plants, green algae), but that are absent or poorly conserved in non‐photosynthetic/heterotrophic organisms. InChlamydomonas reinhardtii,CPLD49 (Conserved inPlantLineage andDiatoms49) is an uncharacterized GreenCut protein that is critical for maintaining normal photosynthetic function. We demonstrate that acpld49mutant has impaired photoautotrophic growth under high‐light conditions. The mutant exhibits a nearly 90% reduction in the level of the cytochromeb₆fcomplex (Cytb₆f), which impacts linear and cyclic electron transport, but does not compromise the ability of the strain to perform state transitions. Furthermore,CPLD49 strongly associates with thylakoid membranes where it may be part of a membrane protein complex with another GreenCut protein,CPLD38; a mutant null forCPLD38 also impacts Cytb₆fcomplex accumulation. We investigated several potential functions ofCPLD49, with some suggested by protein homology. Our findings are congruent with the hypothesis thatCPLD38 andCPLD49 are part of a novel thylakoid membrane complex that primarily modulates accumulation, but also impacts the activity of the Cytb₆fcomplex. Based on motifs ofCPLD49 and the activities of otherCPLD49‐like proteins, we suggest a role for this putative dehydrogenase in the synthesis of a lipophilic thylakoid membrane molecule or cofactor that influences the assembly and activity of Cytb₆f.