Genetic structures surrounding the carbapenem-hydrolyzing oxacillinase gene blaOXA-58 were characterized in a series of OXA-58-positive Acinetobacter baumannii strains isolated from different countries. We showed that in most of the cases, acquisitions of the blaOXA-58-containing overall structure, including insertion sequence elements, may be likely the results of recombination events. In type strain A. baumannii MAD, the genetic structure surrounding the blaOXA-58 gene was bracketed by two 27-bp repeated sequences. The isolation of a clonally related OXA-58-negative A. baumannii isolate that possessed the same plasmid backbone as A. baumannii MAD but lacked this genetic structure indicated that the mechanism of acquisition could be reversible. Parts of the structure identified in A. baumannii MAD were conserved in other blaOXA-58-positive isolates from various European countries. Primer extension experiments showed that blaOXA-58 expression was related to promoter sequences brought by different insertion sequence elements, such as an ISAba3-like element, ISAba1, ISAba2, and IS18. This work identified novel structures at the origin of acquisition and expression of a carbapenem-hydrolyzing beta-lactamase identified in non-clonally related A. baumannii isolates.