A key step in most viral infections is the binding of a viral protein to a host receptor, leading to the virus entering the host cell. Disrupting this protein-protein interaction is an effective strategy for preventing infection and subsequent disease. Building on recent advances in computational tools for structural biology, we introduce Virus Inhibition via Peptide Engineering and Receptor Mimicry (VIPER), a novel approach for the automatic derivation and optimization of biomimetic decoy peptides that mimic binding sites of human proteins. VIPER leverages structural data from human-pathogen protein complexes, yielding peptides that can competitively inhibit viral entry by mimicking the natural receptor. We computationally validated VIPER using molecular dynamics simulations and showcased its applicability on three clinically relevant viruses, highlighting its potential to accelerate therapeutic development. With a focus on reproducibility and extensibility, VIPER can facilitate the rapid development of antiviral inhibitors by automating the design and optimization of biomimetic compounds.