The breast is a dynamic organ whose response to physiological and pathophysiological conditions alters its disease susceptibility, yet the specific effects of these clinical variables on cell state remain poorly annotated. We present a unified, high-resolution breast atlas by integrating single-cell RNA-seq, mass cytometry, and cyclic immunofluorescence, encompassing a myriad of states. We define cell subtypes within the alveolar, hormone-sensing, and basal epithelial lineages, delineating associations of several subtypes with cancer risk factors, including age, parity, and BRCA2 germline mutation. Of particular interest is a subset of alveolar cells termed basal-luminal (BL) cells, which exhibit poor transcriptional lineage fidelity, accumulate with age, and carry a gene signature associated with basal-like breast cancer. We further utilize a medium-depletion approach to identify molecular factors regulating cell-subtype proportion in organoids. Together, these data are a rich resource to elucidate diverse mammary cell states. [Display omitted] • Multimodal single-cell analyses identify breast epithelial and stromal subtypes • Spatially distinct epithelial subsets are linked with age, parity, and BRCA2 status • Alveolar cells with poor transcriptional lineage fidelity accumulate with age • Subtypes of the three major epithelial lineages are maintained in organoid cultures Gray, Li, Rosenbluth, Selfors et al. generate a multi-dimensional atlas of breast tissues and organoids. Distinct epithelial subtypes are found to be associated with age, parity, and BRCA2 mutation. An alveolar subset termed basal-luminal cells displays poor transcriptional lineage fidelity and gene expression signatures associated with aggressive basal-like breast cancers. [ABSTRACT FROM AUTHOR]