The mechanism of the unique arylpropionate racemase AMDase G74C was investigated by a QM/MM approach. Molecular dynamics simulations showed that the mechanism is initiated by a deprotonation of the catalytic cysteine. The simulations revealed two thiolate pockets. While the first plays a role in the natural decarboxylative activity of AMDase, the second stabilizes the artificially introduced thiolate group of C74. The presence of the two structural motifs is a prerequisite for the promiscuous racemization reaction of AMDase G74C. QM/MM simulations show that the deprotonation and reprotonation proceed in a stepwise fashion, in which a planar enedionate intermediate is stabilized by a delocalized π-electron system on a vinylic or aromatic substituent of the substrate. The artificial racemase is thus a typical case of substrate-assisted catalysis.