Accurate knowledge of breast duct anatomy in three dimensions is needed to understand normal breast development, how intraepithelial neoplasia may spread through a breast, and the potential for diagnostic and therapeutic access to breast parenchyma via the nipple. This paper reports three related exploratory studies. In study 1, the median number of milk-collecting ducts in the nipple was determined in 72 breasts excised for cancer; in study 2, the volumes of all 20 complete duct systems (‘lobes’) in an autopsy breast were measured from 2 mm serial ‘subgross’ sections; and in study 3, a 3D digital model of all collecting ducts in a mastectomy nipple was made from 68 100 µm serial sections. The mastectomy nipples contained 11–48 central ducts (median 27, inter-quartile range 21–30). In the autopsy breast, the largest ‘lobe’ drained 23% of breast volume; half of the breast was drained by three ducts and 75% by the largest six. Conversely, eight small duct systems together accounted for only 1.6% of breast volume. The 3D model of the nipple revealed three distinct nipple duct populations. Seven ducts maintained a wide lumen up to the skin surface (population A); 20 ducts tapered to a minute lumen at their origin in the vicinity of skin appendages (population B) on the apex of the nipple; and a minor duct population (C) arose around the base of the papilla. Major variations in duct morphology and extent define highly variable territories in which intraepithelial neoplasia could grow. While population A ducts appear accessible to duct endoscopy or lavage, population B and population C ducts may be less accessible. Copyright © 2004 Pathological Society of Great Britain and Ireland. Published by John Wiley & Sons, Ltd.