Significance Land plants produce numerous terpenoids that regulate development and mediate environmental interactions. Thus, how typical plant terpene synthase ( TPS ) genes originated and evolved to create terpenoid diversity is of fundamental interest. By investigating TPSs from the genomes and transcriptomes of diverse taxa of green plants, it was demonstrated here that the ancestral TPS gene originated in land plants after divergence from green algae and encoded a bifunctional ent -kaurene synthase for phytohormone biosynthesis. This ancestral TPS then underwent gene duplication at least twice early in land plant evolution, leading to three ancient TPS lineages reflecting sub-functionalization of class I and II activities for phytohormone biosynthesis and neo-functionalization from primary to secondary metabolism, followed in each case by dynamic functional divergence.