The exon junction complex (EJC) plays important developmental roles in animals; however, its role in plants is not well known. Here, we show various aspects of divergence of each duplicated MAGO- and Y14-gene pair in rice encoding the putative EJC core subunits that form the obligate MAGO-Y14 heterodimers. OsMAGO1, OsMAGO2 and OsY14a were constitutively expressed in all tissues while OsY14b was predominantly expressed in embryonic tissues. OsMAGO2 and OsY14b were more sensitive to different stresses than OsMAGO1 and OsY14a, and their encoded protein pair shared 93.8% and 46.9% sequence identity, respectively. Single MAGO downregulation in rice did not lead to any phenotypic variation; however, double-gene knockdowns generated short rice plants with abnormal flowers, and the stamens of these flowers showed inhibited degradation and absorption of both endothecium and tapetum, suggesting that OsMAGO1 and OsMAGO2 were functionally redundant. OsY14a knockdowns phenocopied OsMAGO1OsMAGO2 mutants while downregulation of OsY14b failed to induce plantlets, suggesting the functional specialization of OsY14b in embryogenesis. OsMAGO1OsMAGO2OsY14a triple downregulation enhanced the phenotypes of OsMAGO1OsMAGO2 and OsY14a downregulated mutants, indicating that they exert developmental roles in the MAGO-Y14 heterodimerization mode. Modified gene expression was noted in the altered developmental pathways in these knockdowns, and the transcript splicing of OsUDT1, a key regulator in stamen development was uniquely abnormal. Concomitantly, MAGO and Y14 selectively bound to the OsUDT1 pre-mRNA, suggesting that rice EJC subunits regulate splicing. Our work provides novel insights into the function of the EJC locus in growth, development and reproduction in angiosperms, and suggests a role for these genes in the adaptive evolution of cereals.