Histidine (His) photo-oxidation has been widely investigated with several transient and stable products characterized, especially for aerobic conditions. Due to its role and structure, His-side chain can be a key player in the quenching of excited states such as the triplet state of the photosensitizer 3-carboxybenzophenone (3CB*). The capacity of His and its derivatives to quench 3CB* under anaerobic conditions are characterized in the current study by laser flash photolysis, with the resulting oxidation products examined by mass spectrometry to determine the reaction mechanism. The latter include adducts of the 3-carboxybenzophenone ketyl radical (CBH•) to the imidazole ring (Imid-CH2-CBH), His-His dimers, and other products with lower yields. The data obtained with model compounds are compared to those obtained with more complicated systems, including the peptide Exendin-4, and the protein MtHpt1. The data obtained from transient spectroscopy and product analyses indicate that two CB* quenching mechanisms occur: (i) proton-coupled electron transfer (as reported previously) yielding radicals that can recombine to give His-His dimers and CBH-adducts, and (ii) energy transfer yielding 3His* undergoing further reaction leading to formation of Imidazyl-CH2-CBH adduct. The latter, unexpected process only occurs when His and its derivatives have a free α-amino group. This process yielded a novel adduct between the imidazole ring and the CBH• formed by sensitizer reduction.