Despite the major advances in breast cancer management over the past few decades, metastatic breast cancer continues to be a major concern and the main cause of mortality associated with this disease. The Rho GTPase RAC1 has been implicated in breast cancer aggressiveness, yet the mechanisms underlying its prometastatic activity remain poorly understood. Although RAC1 overexpression is correlated with poor prognosis, our data indicate that increased abundance alone is insufficient to drive metastatic dissemination in preclinical models. While RAC1 overexpression in MMTV-ErbB2 mice accelerates primary tumor growth, it does not increase metastasis. Using complementary genetic models, we show that disrupting RAC1 SUMOylation reduces lung metastases; this uncoupling from primary tumor development is clearest in the RAC1K4R knock-in model, whereas the RAC1ΔSUMO1 transgenic mice also show partial attenuation of RAC1-driven proliferative signaling. Mechanistically, loss of SUMOylation impaired the ability of RAC1 to maintain its GTP-bound state in proinvasive contexts. To exploit this dependency, we developed a cell-permeable peptide, TAT-PRASI, that blocks RAC1 SUMOylation. TAT-PRASI decreases RAC1 activity and limits migration/invasion in vitro and metastasis in vivo while reducing the invasion of patient-derived organoids. Moreover, TAT-PRASI diminishes the RAC1-POTEE interaction, which is consistent with impaired invadopodia formation. Collectively, these findings identify SUMOylation as a specific, druggable regulator of RAC1-driven metastasis, providing a preclinical proof-of-concept for selectively targeting this posttranslational modification in metastatic breast cancer.