Updated project metadata. • Polycomb (PcG) regulation is crucial for development across eukaryotes, but how PcG targets are specified is still incompletely understood. The slow timescale of cold-induced Polycomb Repressive Complex 2 silencing during vernalization at Arabidopsis thaliana FLOWERING LOCUS C (FLC) provides an excellent system to elucidate the sequence of events. Association of the DNA binding protein VAL1 to an FLC intronic RY motif within the PcG nucleation region is an important step. VAL1 is associated in vivo with APOPTOSIS AND SPLICING ASSOCIATED PROTEIN (ASAP) complex and Polycomb Repressive Complex 1 (PRC1). Here, we show that ASAP and PRC1 functions are necessary for co-transcriptional repression and chromatin regulation during FLC silencing. ASAP mutants affect FLC transcription in warm conditions, but the rate of FLC silencing in the cold is unaffected. PRC1-mediated H2Aub accumulation increases at the nucleation region upon exposure to cold, but unlike the PRC2-delivered H3K27me3 does not spread across the locus. H2Aub is thus involved in the transition to epigenetic silencing at FLC facilitating H3K27me3 accumulation, which in turn is necessary for long-term epigenetic memory. Overall, our work highlights the importance of the DNA sequence-specific binding protein VAL1 as an assembly platform coordinating the co-transcriptional repression and chromatin regulation necessary for the epigenetic silencing of FLC.