SignificanceStudies of PRC2 in vitro indicate that RNA inhibits its histone methyltransferase (HMTase) activity through mutually antagonistic binding with nucleosomes, but some in vivo studies paradoxically suggest that RNA binding is necessary to facilitate its chromatin occupancy and HMTase activity. Our findings unveil a mechanism for direct exchange of RNA and DNA/nucleosome on the PRC2 protein complex, which reconciles these prior findings by allowing RNA regulation of PRC2 to be antagonistic or synergistic depending on RNA–nucleosome proximity. Furthermore, there is an increasing awareness that multiple chromatin-associated proteins exhibit regulatory RNA binding activity, and our findings indicate that this “direct transfer” mechanism may be generally required for RNA recruitment of proteins to chromatin.