Breast cancer (BC) prognosis and outcome are adversely affected by obesity. Hyperinsulinemia, common in the obese state, is associated with higher risk of death and recurrence in BC. Up to 80% of BCs overexpress the insulin receptor (INSR), which correlates with worse prognosis. INSR’s role in mammary tumorigenesis was tested by generating MMTV-driven polyoma middle T (PyMT) and ErbB2/Her2 BC mouse models, respectively, with coordinate mammary epithelium-restricted deletion of INSR. In both models, deletion of either one or both copies of INSR leads to a marked delay in tumor onset and burden. Longitudinal phenotypic characterization of mouse tumors and cells reveals that INSR deletion affects tumor initiation, not progression and metastasis. INSR upholds a bioenergetic phenotype in non-transformed mammary epithelial cells, independent of its kinase activity. Similarity of phenotypes elicited by deletion of one or both copies of INSR suggest a dose-dependent threshold for INSR impact on mammary tumorigenesis. Display omitted •Insulin receptor (INSR) is broadly expressed in breast cancer (BC)•INSR deletion suppresses mammary tumorigenesis driven by Her2 and PyMT oncogenes•INSR affects tumor initiation, not progression and metastasis•INSR upholds bioenergetic fitness of mammary epithelial cells Insulin receptor (INSR) is found in most human breast cancers. Podmore et al. demonstrate that INSR contributes to cancer development in two mouse models representing major human breast cancer types by affecting the earliest stages of tumor development. Mechanistically, INSR supports cellular energy production necessary for malignant transformation.