We previously found that the RING-type E3 ligaseDEFECTIVE IN ANTHER DEHISCENCE1-(DAD1-) Activating Factor(DAF)controls anther dehiscence by activating the jasmonate biosynthetic pathway inArabidopsis. Here, we show that inArabidopsis, theDAFancestor was duplicated into three genes (DAF, Ovule Activating Factor (OAF), DAFL2), which evolved divergent partial functions from their ancestor through subfunctionalization. In this case, DAF-DAD1-JA signaling regulates anther dehiscence, whereasOAFcontrols ovule development by negatively regulating cinnamyl alcohol dehydrogenase 9 (CAD9) activity and being negatively regulated by miR847 itself inArabidopsis. Downregulation ofOAFor upregulation ofCAD9and miR847 caused similar abortion of ovule formation due to precocious ovule lignification in transgenicArabidopsis. Interestingly, only oneDAF-like gene,PaOAF, exists in the monocot orchids, which has likely evolved through nonfunctionalization and maintains a conserved function asArabidopsis OAFin regulating ovule development since defective ovules were observed in the virus-induced gene silencing (VIGS)PaOAF Phalaenopsisorchids. The absence of theDAFortholog and its function in orchids is likely due to the evolution of stamens to a unique pollinium structure that lacks the feature of anther dehiscence. These findings expand the current knowledge underlying the multifunctional evolution and diverse functionalization of duplicate gene pairs within/among plants.