Phenotypic plasticity is a hallmark of cancer which underlies many aspects of cancer evolution, metastasis, and therapy resistance; however the molecular basis of this plasticity remains elusive. Bivalent chromatin, defined by the co-occurrence of active-associated trimethyl-lysine 4 on histone H3 (H3K4me3) and repressive-associated trimethyl-lysine 27 on histone H3 (H3K27me3) histone modifications on the same nucleosome is well-defined marker of molecular plasticity in embryonic cells where it marks poised developmental genes required for differentiation. In breast cancer, bivalency is linked to chemo-resistance and enhanced tumorigenicity, however detailed understanding of distribution and function in breast cancer is lacking. This is partly due to the technical challenges distinguishing bone-fide bivalency, where both marks are on the same nucleosome, from allelic or cellular heterogeneity where there is a mix of H3K4me3-only and H3K27me3-only mono-nucleosomes. Here, we use our recently published robust ChIP-reChIP protocol to accurately map bivalent chromatin genome-wide in non-transformed mammary epithelial cells, alongside a series of breast cancer cell lines. While comparison of our reChIP method within silico approaches revealed high concordance between approaches the reChIP displayed a higher sensitivity in detecting bivalent regions. Interestingly, we uncover breast cancer sub-type specific bivalent chromatin signatures suggesting this chromatin state is dynamic and varies between cellular contexts. Our findings provide insight into how bivalent chromatin may prime transcriptional networks of biological and clinical importance while also enhancing our understanding of the fundamental molecular processes driving plasticity in breast cancer.