Five peptide ligands of four different cell surface receptors (nucleolin, CXCR1 CMKLR1 and CD44v6) have been evaluated as targeting moieties for triple-negative human breast cancers. Among them, the peptide F3, derived from phage display, promotes the fast and efficient internalization of a genetically fused GFP inside MDA-MB-231 cancer stem cells, in a specific receptor-dependent fashion. The further engineering of this protein into the modular construct F3-RK-GFP-H6 and the subsequent construct F3-RK-PE24-H6, resulted in self-assembling polypeptides that organize as discrete and regular nanoparticles. These materials, of 15-20 nm in size, show enhanced nucleolin-dependent cell penetrability. We show that the F3-RK-PE24-H6, based on the Pseudomonas aeruginosa exotoxin A (PE24) as a core functional domain, is highly cytotoxic over target cells. The combination of F3, the cationic peptide (RK)n, and the toxin domain PE24 in such unusual presentation appears as a promising approach to cell-targeted drug carriers in breast cancers and address selective drug delivery in otherwise difficult-to-treat triple-negative breast cancers.