The blue light using flavin (BLUF) domain is one of nature’s smallest photoswitching protein domains, yet a cross-species photoactivation mechanism is lacking. Its photoactivation involves an intricate bidirectional proton-coupled electron transfer (PCET) reaction; however, the key reverse PCET route remains largely elusive, with its elementary steps undissected. Here, we resolved the light-state photoreaction cycles of the BLUF domains in 3 species, i.e., AppA from Rhodobacter sphaeroides, OaPAC from Oscillatoria acuminata, and SyPixD from Synechocystis sp. PCC6803, with a unified kinetic model. Using mutant design and femtosecond spectroscopy, we captured the spectroscopic snapshots of a key proton-relay intermediate in all species, revealing that the light-state photoreaction cycle consists of 4 elementary steps including a forward concerted electron-proton transfer (CEPT), a 2-step proton rocking, and a reverse CEPT. We emphasize that the last reverse CEPT step (1.5 to 3.7 ps) is shared by both the light-state and dark-state photocycles and is essential to the photoswitching functionality.