The light-driven water-splitting reaction of photosystem II exposes its key reaction center core protein subunits to irreversible oxidative photodamage. A rapid repair cycle replaces the photodamaged core subunits in plants, but how the large antenna-core supercomplex structures of plant photosystem II disassemble for repair is not currently understood. Here, we report the specific involvement of phosphorylation in removal of the peripheral antenna from the core and monomerization of the dimeric cores. However, monomeric cores disassemble further into smaller subcomplexes, even in the absence of phosphorylation, suggesting that there are other unknown mechanisms of disassembly. In this regard, we show that oxidative modifications of amino acids in core protein subunits of photosystem II are active mediators of monomeric core disassembly. Oxidative modifications thus likely disassemble only the damaged monomeric cores, ensuring an economical photosystem disassembly process. Taken together, our results suggest that phosphorylation and oxidative modification play distinct roles in photosystem II disassembly and repair.