The genome of the industrially important fungus Aspergillus niger encodes a large number of glycoside hydrolase family 18 members annotated as chitinases. We identified one of these putative chitinases, CfcI, as a representative of a distinct phylogenetic clade of homologous enzymes conserved in all sequenced Aspergillus species. Where the catalytic domain of more distantly related chitinases consists of a triosephosphate isomerase barrel in which a small additional (α+β) domain is inserted, CfcI-like proteins were found to have, in addition, a carbohydrate-binding module (CBM18) that is inserted in the (α+β) domain next to the substrate-binding cleft. This unusual domain structure and sequence dissimilarity to previously characterized chitinases suggest that CfcI has a novel activity or function different from chitinases investigated so far. Following its heterologous expression and purification, its biochemical characterization showed that CfcI displays optimal activity at pH 4 and 55-65 °C and degrades chitin oligosaccharides by releasing N-acetylglucosamine from the reducing end, possibly via a processive mechanism. This is the first fungal family 18 exochitinase described, to our knowledge, that exclusively releases monomers. The cfcI expression profile suggests that its physiological function is important in processes that take place during the late stages of the aspergillus life cycle, such as autolysis or sporulation.