The flexibility of the spatio-temporal genome replication program during development and disease highlights the regulatory role of plastic epigenetic mechanisms over genetic determinants. Histone post-translational modifications have been broadly implicated in replication timing control, yet the specific mechanisms through which individual histone marks influence replication dynamics, particularly in heterochromatin, remain unclear. Here, we demonstrate the dynamic enrichment of H3K36me3 at pericentromeric constitutive heterochromatin (chromocenters) consisting of major satellite (MaSat) repeats preceding replication during the S II sub-phase of the S phase in mouse embryonic stem cells. Through the knockdown of lysine 36 specific methyltransferases or targeted introduction of oncohistone to chromocenters, we reduced both global or local H3K36me3 levels, respectively, revealing its essential role in preserving the replication timing of constitutive heterochromatin. Loss of H3K36me3 was accompanied by reduced MaSat RNA levels and increased RNA polymerase II serine-5 phosphorylation, indicating transcriptional dysregulation. Notably, we identify a strand-specific contribution of MaSat forward transcripts in fine-tuning replication timing and maintaining chromatin stability, highlighting non-coding RNA as a critical regulator of replication timing.