High-grade serous ovarian cancer (HGSC), the most lethal subtype of ovarian cancer, is now widely accepted to originate from the fallopian tube (FT) epithelium. This subtype is also the most commonly diagnosed in individuals carrying BRCA1 mutations. However, the specific cell population responsible for tumour initiation within the FT remains unidentified. Despite its importance, this is understudied tissue with lack of characterization of the differentiation hierarchy and the FT stem cells, which are the most likely candidates to be the cell-of-origin of ovarian cancer. 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 genetically engineered mouse models, lineage tracing 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 and locations, including a stem cell niche. 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.