Vitamin D deficiency is common in breast cancer patients and some evidence suggests that low vitamin D status enhances the risk for disease development or progression. In addition to receptors for classic steroid hormones such as estrogen and progesterone, the vitamin D receptor (VDR) and its ligand 1,25(OH)2D modulate normal mammary gland development and sensitivity to carcinogenesis. Genomic profiling has characterized many 1,25(OH)2D responsive targets in normal mammary cells and in breast cancers, providing insight into the molecular actions of 1,25(OH)2D and the VDR in regulation of cell cycle, apoptosis and differentiation. Newer areas of emphasis regarding the effects of vitamin D on breast cancer include its effects on estrogen signaling, cellular metabolism and cancer stem cells. Here we present a model of vitamin D pathway evolution during mammary cell lineage development which predicts heterogeneous VDR expression in differentiated populations. This model is supported by analysis of single cell datasets from normal breast tissue which demonstrates several distinct VDR positive glandular cell populations. We note that CYP27B1 strongly co-localizes with VDR in glandular cells, but that CYP24A1 is most highly expressed in a distinct glandular cell population. All of these glandular cell populations are theoretically susceptible to carcinogenesis, leading to breast cancers with heterogeneity in VDR pathway activity. The relevance of the vitamin D pathway in human breast tumors was evaluated by annotation of copy number alterations (CMAs) and altered mRNA expression of VDR, CYP24A1 and CYP27B1 in publicly accessible datasets in relation to clinical outcomes including survival. These data highlight the complexity of VDR signaling in both normal mammary gland and in breast cancers.