Mineralization of aromatic compounds—present in large amounts in the biosphere—is a challenging chemical process. Nature developed several sophisticated degradation strategies, one of them being the benzoate‐degrading CoA‐linked Box pathway that is present in 5% of all sequenced bacterial genomes. The central dearomatization and cleavage reaction is accomplished by the BoxABC multicomponent system; BoxA is a reductase, BoxB an epoxidase using a single O 2 molecule, and BoxC a stimulator for the BoxB reaction and a hydrolase for subsequent ring cleavage. BoxB is a member of the important diiron carboxylate protein family characterized by a catalytic diiron center embedded in a central four‐helix bundle. Benzoyl‐CoA is located inside a 20 Å long channel of BoxB. The position of its phenyl ring relative to the diiron center is accurately defined in the X‐ray structure and allowed valuable insight into O 2 binding and activation, epoxidation, and the stereoselectivity of the reaction. Kinetic‐ and electron paramagnetic resonance (EPR)‐spectroscopic investigations provided information about the reaction dynamics and reaction intermediates. On the basis of the total data available, a detailed enzymatic mechanism is proposed.