The cytochrome b6f complex (b6f) links photosystem II and photosystem I in photosynthetic electron transfer and is distributed between appressed and non-appressed thylakoid membranes. It also activates the state-transition 7 kinase (STT7), which phosphorylates light-harvesting complex proteins, facilitating energy redistribution between photosystems to optimize their efficiency. To investigate the role of STT7-dependent phosphorylation at T4 in the N-terminal domain of the b6f subunit-IV (PetD), we generated several chloroplast mutants. The phosphomimic mutation PetD T4E blocks STT7 kinase activity since proteomics show the absence of STT7-dependent phosphorylation and the strain being locked in State 1, revealing a novel feedback regulation mechanism. The deletion of five N-terminal amino acids resulted in a comparable inhibition of STT7 activity; furthermore, the additional disruption of electron transfer underscores an additional crucial role of the PetD N-terminus in b6f function.