Canonical Polycomb Repressive Complex 1 (cPRC1) preserves cell fate decisions by repressing inappropriate transcription of developmental regulator genes. We report the cryo–electron microscopy structure of tetrameric human cPRC1 bound to a nucleosome, in complex with native ubiquitin-conjugating enzyme UBCH5C. cPRC1 adopts a compact architecture, orchestrated by the PHC2HD domain which is sandwiched between BMI1 and a structural lobe formed by the CBX7C-box and RING1BRAWUL domains. In this compact conformation, RING1B, BMI1 and PHC2 form an extended interface that stably positions UBCH5C on the nucleosome to enable efficient monoubiquitination of histone H2A at lysine 119 (H2Aub1). This tightly organized architecture is conserved in Drosophila cPRC1, where mutational analyses establish the Polyhomeotic (Ph) subunit as the key scaffolding and targeting factor. While the PhHD domain is critical for complex assembly, the PhSAM domain is dispensable for assembly but essential for recruiting cPRC1 to target genes, a prerequisite for cPRC1-mediated H2A monoubiquitination