The mammary gland is a very dynamic organ that matures during puberty to a state poised for development during pregnancy and lactation. The ductal system is composed of an epithelial bilayer of basal and luminal cells: mammary stem cells are found within the outer basal layer, whilst the inner luminal layer comprises progenitor pools and hormone sensing, mature luminal cells. Transcriptional regulation is a complex and multifaceted biological process. Cis-regulatory elements are responsible for complex fine-tuning of gene expression in a tissue-specific manner. In the mammary gland, many questions remain as to how gene regulation defines each of the epithelial lineages and the nature of their chromatin. We sought to systematically characterise the transcriptomic and epigenetic landscape of the different epithelial cells, uncovering key differences in lineage chromatin profiles. Using chromatin looping techniques, we show that lineage gene regulation is linked to priming and de novo activation of enhancers and uncover an extensive involvement of polycomb silencer regions. We further show that alternative transcriptional start site (TSS) usage is influenced by chromatin interactions and that TSS interactivity is highly cell dependent. These data demonstrate that within the adult mammary gland, basal cells prime luminal genes for expression during differentiation, whilst basal genes are heavily repressed within luminal cells. This body of work provides an atlas of the epigenetic state of mammary epithelial cells and identifies novel regulators of lineage fidelity.