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Here, we uncover I\u03baB\u03b1 (<jats:italic>Nfkbia<\/jats:italic>, the inhibitor of NF-\u03baB) as a critical regulator of HSC proliferation throughout development. I\u03baB\u03b1 balances retinoic acid signaling levels together with the epigenetic silencer, PRC2, specifically in HSCs. Loss of <jats:italic>I\u03baB\u03b1<\/jats:italic> decreases proliferation of HSC and induces a dormancy related gene expression signature instead. Also, I\u03baB\u03b1 deficient HSCs respond with superior activation to in vitro culture and in serial transplantation. At the molecular level, chromatin regions harboring binding motifs for retinoic acid signaling are hypo-methylated for the PRC2 dependent H3K27me3 mark in I\u03baB\u03b1 deficient HSCs. 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