Recently, the seminal discovery that metastatic breast cancer cells up-regulate DNA damage repair proteins in order to stabilize an unstable genome has sparked substantial interest in deciphering the mechanisms supporting cancer progression and targeting these molecules therapeutically. We have identified a key homologous recombination (HR) DNA repair protein, RAD51 that is overexpressed in patient breast metastases samples compared to matched primary breast cancer. We find depletion of RAD51 inhibited metastases in a murine, syngeneic breast cancer model and xenograft transplants. Corresponding with inhibition of metastasis we observed changes in cell morphology, pro-metastatic gene expression profile and immune signaling. We believe RAD51 is functioning as a transcriptional co-factor influencing three related mechanisms via changes in expression of; Rho and Rac GTPases affecting actin dynamics, matrix-metallo-proteases affecting interaction with the surrounding environment, and chemokine receptor CXCR4 affecting cell signaling. The combination of these influences results in effective inhibition of metastasis at multiple functional levels. This demonstrates for the first time a new activity for RAD51 that may underlie the proclivity of patients with RAD51 overexpression to develop distant metastasis. Therefore we suggest RAD51 is a potential biomarker and attractive drug target for metastatic cancers.