Fatty acids (FAs) are major building blocks of membrane phospholipids in bacteria and eukaryotes. Their presumed absence in archaea led to propose a late origin in bacteria and eukaryotes and that the last common ancestor of living organisms (the cenancestor) was devoid of both FA and phospholipid membranes. However, small FA amounts and homologs of bacterial FA biosynthesis enzymes are found in archaea. We have investigated the origin of these archaeal enzymes using phylogenomic analyses of all enzymes of the main bacterial FA biosynthesis pathway. Our results suggest that modern archaea and their last common ancestor possessed a complete pathway except for the acyl carrier protein (ACP) processing machinery, which evolved in the bacterial lineage. This has not only implications for archaeal physiology but also opens the possibility for the presence of ACP-independent FA synthesis in the cenancestor, which may have been endowed with FA-phospholipid membranes.