The Polycomb Repressive Complex 2 (PRC2) is a chromatin regulatory complex essential for development and maintenance of cellular identity in multicellular organisms. PRC2 is composed of core subunits EED, SUZ12 and EZH1/2, which together mediate all mono-, di-, and tri-methylation of lysine 27 on histone H3 (H3K27me1/2/3). The activity of PRC2 is perturbed in multiple cancers and small-molecule inhibitors have been developed and used to treat cancer. Here, we discover that a distinct form of PRC2 predominates in quiescent cells, containing EZH1, EED, SUZ12 and the Polycomb-like protein, PHF1, but crucially lacks EZH2. This distinct form of PRC2 functions independently of catalytic activity to maintain H3K27me2/3 levels, and repress key Polycomb target genes in quiescent cells. We also show that key members of canonical PRC1 (cPRC1) are transcriptionally upregulated and enriched on Polycomb target genes in quiescent cells, and this coinciding with an increase in chromatin compaction at these sites. Loss of EZH1-PRC2 in quiescent cells by treatment with an EED chemical degrader results in loss of cPRC1 binding and derepression of some PcG target genes. Our results uncover a novel synergy between EZH1-PRC2 and cPRC1 and elegantly demonstrate that EZH1-PRC1 functions independently of catalytic activity in quiescent cells. These results provide a cautionary note for the use of PRC2 inhibitors in the treatment of cancers that contain dormant non-proliferating cancer cells.