Hereditary breast cancers are frequently caused by germline BRCA1 mutations. The BRCA1^C61G mutation in the BRCA1 RING domain is a common pathogenic missense variant, which reduces BRCA1/BARD1 heterodimerization and abrogates its ubiquitin ligase activity. To investigate the role of BRCA1 RING function in tumor suppression and therapy response, we introduced the Brca1^C61G mutation in a conditional mouse model for BRCA1-associated breast cancer. In contrast to BRCA1-deficient mammary carcinomas, tumors carrying the Brca1^C61G mutation responded poorly to platinum drugs and PARP inhibition and rapidly developed resistance while retaining the Brca1^C61G mutation. These findings point to hypomorphic activity of the BRCA1-C61G protein that, although unable to prevent tumor development, affects response to therapy.