Small heat shock proteins (sHSPs) are chaperones that play an important role in stress tolerance. They consist of an alpha-crystallin domain (ACD) flanked by N- and C-terminal regions. However, not all proteins that contain an ACD, hereafter referred to as ACD proteins, are sHSPs because certain ACD proteins are known to have different functions. Furthermore, since not all ACD proteins have been identified yet, current classifications are incomplete. A total of 17 complete plant proteomes were screened for the presence of ACD proteins by HMMER profiling and the identified ACD protein sequences were classified by maximum likelihood phylogeny. Differences among and within groups were analysed, and levels of functional constraint were determined. There are 29 different classes of ACD proteins, eight of which contain classical sHSPs and five likely chaperones. The other classes contain proteins with uncharacterised or poorly characterised functions. N- and C-terminal sequences are conserved within the phylogenetic classes. Phylogenetics suggests a single duplication of the CI sHSP ancestor that occurred prior to the speciation of mono- and dicotyledons. This was followed by a number of more recent duplications that resulted in the presence of many paralogues. The results suggest that N- and C-terminal sequences of sHSPs play a role in class-specific functionality and that non-sHSP ACD proteins have conserved but unexplored functions, which are mainly determined by subsequences other than that of the ACD.