Metastatic melanoma remains a highly lethal cancer, largely due to the rapid emergence of resistance to current therapies. Despite recent advances with targeted therapies and immune checkpoint inhibitors, many patients fail to respond or relapse within months due to acquired drug resistance. To address this challenge, we investigated a novel therapeutic approach using membrane-disruptive cyclic peptides to eliminate melanoma cells that evade conventional treatments. Our study profiled lipidomic and proteomic changes in melanoma cells during the development of resistance to dabrafenib, a BRAF inhibitor used in BRAFV600E-positive melanoma. We then evaluated the efficacy of two cyclic peptides, cyclic tachyplesin I (cTI) and cyclic gomesin (cGm) which exhibit rapid, membrane-targeted cytotoxicity. These peptides effectively eliminated drug-naïve, drug-tolerant, and drug-resistant melanoma cells in vitro, without inducing further resistance even upon prolonged exposure of cTI. Notably, in a mouse model, combination therapy with cTI and dabrafenib reduced metastatic burden and improved overall survival compared to dabrafenib alone. Our findings support the potential of cyclic peptides to be developed both as standalone agents and in combination therapy to overcome resistance and improve outcomes in metastatic melanoma.