Elastin-derived peptides (EDPs) interact with elastin-binding protein (EBP), a key component of the elastin receptor complex, modulating cellular processes such as protease activation, apoptosis, and chemotaxis via regulation of NEU-1 sialidase activity. Despite their therapeutic relevance, the structural basis of EDP-EBP interactions remains poorly understood. Here, we present the first full-length homology model of EBP (residues 29–516), constructed and validated through duplicate 1 microsecond long molecular dynamics (MD) simulations. Molecular docking of VGVAPG (as a representative EDP) and lactose (as a representative galactosugar) followed by MD simulations, allowed us to identify key binding residues: D98, E99, S104, and S136 for VGVAPG; and E99, S101, S104, N116, Q124, E137, and Y139 for lactose. These data reveal a shared binding region within residues 83–139, suggesting a competitive binding between EDPs and galactosugars. Furthermore, EBP residues P233 and I234 were implicated in potential interactions with PPCA or NEU-1, contributing to ERC assembly. These findings offer new insights into the molecular recognition mechanisms of EBP and provide a foundation for the design of EBP-targeted elastin peptide antagonists.