Fat tailed sheep breeds are known for their adaptation to nutritional stress, among other harsh production conditions. Damara sheep, native to Southern Africa, have recently been exported to other areas of the world, particularly Australia, aiming to produce lamb in semi-arid regions. Damaras have a unique hanging fat tail, a fat depot able to be mobilized under nutritional stress. In this article we perform an in-depth characterization of the fatty acid profiles of the fat tail in underfed and control Damara rams. Profiles were very similar between experimental groups, with the exception of palmitic acid (16:0) that was lower (P = 0.014) in underfed animals. However, the most striking result was the very high proportions of non-terminal branched chain fatty acids found in the fat tail adipose tissue, as well as the gastrocnemius muscle of Damara rams. The muscle of Dorper and Merino rams used in the same experiment did not present non-terminal branched chain fatty acids, suggesting that Damara rams have a unique lipid metabolism. Herein, we interpret this trait relating it to a higher ability of Damara sheep to digest fibrous fodder and to putative differences in the propionate metabolism by comparison to other sheep breeds.