D-amino acids are the D stereoisomers of common L-amino acids found in proteins. In the past two decades, the occurrence of D-amino acids in plants has been reported and circumstantial evidence for a role in several processes has been provided, including the interaction with soil microorganisms or an interference with cellular signalling. However, examples are relatively scarce and D-amino acids can also be detrimental, some of them inhibiting growth and development. Thus, the persistence of a D-amino acid metabolism in plants is rather surprising and evolutive origins of D-amino acid metabolism is presently unclear. Systemic analysis of sequences associated with enzymes of D-amino acid metabolism shows that they are not simply inherited from cyanobacterial metabolism. In effect, the history of enzymes of plant D-amino acid metabolism likely involves several steps, cellular compartments, gene transfers and losses. Regardless of evolutive steps, enzymes of D-amino acid metabolism like D-amino acid transferases or racemases have been kept by higher plants and not simply eliminated, hence it is likely that they fulfil important metabolic roles, which can be illustrated with serine, tryptophan, and folate metabolism. We suggest that D-amino acid metabolism was perhaps crucial to support metabolic functions required during land plants evolution.