With no new antibiotics on the horizon, understanding the epidemiology of extensively antibiotic resistant Acinetobacter baumannii is becoming increasingly important for infection control and surveillance. In A. baumannii genomes, two large gene clusters direct the synthesis of the immunogenic extra-cellular polysaccharides, capsule (K) and outer core (OC) of the lipooligosaccharide (LOS). It is common for these gene clusters to vary in a species, and examination of >150 publicly available A. baumannii genomes revealed more than 50 distinct capsule gene clusters that include different combinations of modules for complex sugar biosynthesis. Twelve OC gene clusters were also found, and these formed two distinct groups. Though extensive replacement of K and OC gene clusters within clones has not been reported before, our analysis has indicated that these loci are not conserved in isolates belonging to the two major A. baumannii clones that account for most extensively antibiotic resistant isolates. Draft genome sequences of >230 A. baumannii clonal isolates recovered from Australian hospitals between 1996 and 2011 were used to examine the extent of this variation in the predominant clones. Six K and 4 OC forms were found in GC1 isolates, and 6 K and 2 OC types in GC2. Exchanges within these clones indicate sublineages and suggests that alterations to capsule and LOS structures may contribute to clonal success. Natural mutants with insertion sequences interrupting genes were found and used to confirm the role of the OC gene cluster in LOS synthesis. Interestingly, one capsule gene cluster contained a unique module predicted to direct the synthesis of a new nonulosonic acid, and the capsule carbohydrate composition revealed a novel sugar never before reported in a natural biological specimen. The sugar has been tentatively named ‘acinetaminic acid’, and a synthesis pathway proposed.