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Plants use intricate mechanisms to adapt to changing iron conditions because iron is essential and also one of the most limiting nutrients for plant growth. Furthermore, iron is potentially toxic in excess and must be tightly regulated. Previously, we showed that chromatin remodeling via histone 3 lysine 27 trimethylation (H3K27me3) modulates the expression of FIT-dependent genes under iron deficiency in roots. This study builds on our previous findings, showing that H3K27me3 also modulates iron regulation in shoots. In the clf mutant, which lacks the predominant H3K27 tri-methyltransferase, we detected increased iron translocation to shoots under iron deficiency as compared to wild type. Transcriptomic analysis of shoots also revealed differential expression of genes consistent with higher iron levels in clf shoots than wild type shoots under iron-deficient conditions. In addition, we verify that YSL1 and IMA1, two genes involved in signaling iron status from shoots to roots, are direct targets of H3K27me3 and reveal iron-dependent deposition of H3K27me3 on these loci. This study contributes to a better understanding of the molecular mechanisms behind iron regulation in plants, as the effect of PRC2-mediated H3K27me3 on iron homeostasis genes expressed in the shoots has not been previously reported to our knowledge.