Epigenetic silencing of a fraction of ribosomal DNA (rDNA) requires association of the nucleolar chromatin‐remodelling complex NoRC to 150–250 nucleotide RNAs (pRNA) that originate from an RNA polymerase I promoter located in the intergenic spacer separating rDNA repeats. Here, we show that NoRC‐associated pRNA is transcribed from a sub‐fraction of hypomethylated rRNA genes during mid S phase, acting in trans to inherit DNA methylation and transcriptional repression of late‐replicating silent rDNA copies. The results reveal variability between individual rDNA clusters with distinct functional consequences.