Capsular polysaccharide (CPS) is a critical surface structure and principal virulence factor for Acinetobacter baumannii, a nosocomial pathogen of global concern due to resistance to therapeutically suitable antibiotics. Synthesis, assembly and export of the CPS structure is directed by genes located at a large genomic locus that was identified and designated the K locus. Through genetic analysis of more than 1000 A. baumannii genomes, over 100 distinct CPS gene clusters (CPSgc) were found and comprehensively annotated, and a simple nomenclature system was developed. Subsequently, A. baumannii CPSgc were found to share a highly conserved genetic arrangement with genes for CPS export and a gene module for simple sugar biosynthesis flanking a central variable region that can contain one or more of over 20 gene modules for synthesis of complex sugars. Our investigation into this genomic region has lead to several unusual findings, which has involved the complete correlation of CPSgc content with CPS chemical structures in over 20 cases where the structures are available. These discoveries have included the occasional finding of the polymerase gene, required for the construction of the CPS, outside of the K locus within genomic islands that may be mobile. In addition, two unusual sugar synthesis gene modules were shown to direct the synthesis of new nonulosonic acids, acinetaminic acid and 8-epi-acinetaminic acid, that have never been found before in nature. Surprisingly, isolates belonging to the two major global clones that account for most extensively antibiotic resistant isolates were also found to harbour more than 15 different CPSgc each, and CPS exchange in these clones define sublineages that are useful for epidemiological tracking. The examination of the genetics and chemical structures of this important cell surface structure has lead to significant discoveries that have formed a major step towards understanding the biology and epidemiology of A. baumannii.