Women with BRCA1 mutations face a 40% lifetime risk of developing ovarian cancer. High-grade serous ovarian cancers (HGSCs) in these carriers are thought to originate from a rare stem cell population within the fallopian tube (FT) epithelium, but this population remains unidentified. In the FT, ciliated cells that are responsible for transporting fertilized ovules coexist with secretory cells, which produce growth factors and nutrients essential for embryo viability. The stem cell is thought to reside within the secretory cell group. Our project aims to identify and characterize secretory cell subtypes to pinpoint the elusive stem cell population, and the target cells predisposed to developing ovarian cancer. We employed lineage tracing, genetically engineered mouse models with Brca1, Trp53 and Pten deletions in the secretory cells, which are frequently mutated in human HGSC, and organoid cultures to model the FT epithelium in vitro. Single-cell RNA sequencing (scRNA-seq) and imaging were performed at different developmental stages and during tumour progression. Our findings reveal distinct secretory cell subtypes with unique markers, locations, and contributions to both uterine and ovarian tumour formation. By deciphering the cellular composition of the fallopian tube, this research advances our understanding of how BRCA1-associated ovarian cancer originates, offering valuable insights for improving diagnostic and therapeutic strategies.