Identifying causal risk variants and their target genes remains a major challenge in the interpretation of discoveries from Genome-wide Association Studies (GWAS). To refine candidate breast cancer risk genes, we generated a comprehensive regulatory atlas of primary mammary epithelial cells using multiple functional genomic assays. Basal, Progenitor and Mature Luminal cells were isolated from healthy breast tissue from six donors by flow cytometry. We performed H3K27ac-mediated HiChIP, ATAC-seq and RNA-seq in at least four replicates for each cell population, identifying >300,000 chromatin interactions and ~200,000 putative cell type-specific regulatory elements. Integration of this regulatory atlas with breast cancer subtype-specific GWAS data revealed significant heritability enrichment in cell type-specific regulatory regions, particularly in enhancers active in differentiated luminal cells. Combining fine-mapped GWAS data (5,394 candidate causal variants) with cell type-specific gene regulatory profiles nominated 645 potential target genes (average 428 per cell type), enriched in pathways related to mammary gland development, DNA damage response and chromatin organisation. Genes encoding transcription factors including FOXA1, TCF7L2 and ZNF136 emerged as candidate cis-regulated target genes, and strikingly, their binding sites overlapped breast cancer risk variants in active enhancers, suggesting genetic risk may be amplified through cell type-specific regulatory networks. Finally, we generated parallel regulatory profiles using HiChIP, ATAC-seq and RNA-seq and performed Massively Parallel Reporter Assays in commonly used breast cell lines to facilitate prioritisation and functional analyses of cancer risk loci. Together, these analyses highlight the importance of cell type-specific gene regulation in mediating breast cancer risk and provide a valuable resource for functional validation of GWAS target genes in mammary epithelial cells.