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The Old Yellow Enzyme from Ferrovum sp. JA12 (FOYE) displays an unusual thermal stability for an enzyme isolated from a mesophilic organism. We determined the crystal structure of this enzyme and performed bioinformatic characterization to get insights into its thermal stability. The enzyme displays a tetrameric quaternary structure; however, unlike the other tetrameric homologs, it clusters in a separate phylogenetic group and possesses unique interactions that stabilize this oligomeric state. The thermal stability of this enzyme is mainly due to an unusually high number of intramolecular hydrogen bonds. Finally, this study provides a general analysis of the forces driving the oligomerization in Old Yellow Enzymes., (© 2025 The Author(s). PROTEINS: Structure, Function, and Bioinformatics published by Wiley Periodicals LLC.)