Fibroblasts are major stromal components of the breast in normal development and cancer. Their major function is to support tissue structure through the production and remodelling of the extracellular matrix (ECM), which is mainly composed by collagens. They also influence tissue function by secreted cytokines and growth factors, mechanical forces and acting as a reservoir for tissue-specific mesenchymal cells. Single-cell RNA-sequencing have revealed great heterogeneity for cancer-associated fibroblasts (CAFs) and both tumour-supressing and tumour-promoting CAFs have been found. It is believed that CAFs with a tumour-supressing function might be found in earlier stages of tumour development, while tumour-promoting CAFs will be more prevalent at a later stage of oncogenesis. However, because of the plasticity and lack of specific markers for the fibroblast compartment, it has been very challenging to target CAFs in the clinic and functional characterization of fibroblast subsets in breast tissue is still missing. In this study we have interrogated mammary fibroblasts by single-cell transcriptomics across postnatal development (puberty, adult, pregnancy, lactation and involution) and oncogenic transformation (hyperplastic and tumoral stages). We have uncovered four major fibroblast subsets in healthy mammary gland that are also found in the hyperplastic tissue, but in varying proportions. On the other hand, we found tumour-specific fibroblast subsets that could be amenable to reprogramming into a normal-like state. Fibroblast subpopulations have been functionally characterized by Fluorescence-Activated Cell Sorting (FACS), confocal microscopy, CRISPR-Cas9 gene editing and co-culture with breast epithelial cells. Characterization and better understanding of fibroblasts during normal healthy mammary gland development and breast cancer will open new avenues for targeting the stroma for breast cancer treatment.