The formation of the complex between the d-fragment of the complement component C3 (C3d) and the modular complement receptor-2 (CR2) is important for cross-linking foreign antigens with surface-bound antibodies and C3d on the surface of B cells. The first two modules of CR2, complement control protein modules (CCPs), participate in non-bonded interactions with C3d. We have used computational methods to analyze the dynamic and electrostatic properties of the C3d-CR2(CCP1-2) complex. The interaction between C3d and CR2 is known to depend on pH and ionic strength. Also, the intermodular mobility of the CR2 modules has been questioned before. We performed a 10 ns molecular dynamics simulation to generate a relaxed structure from crystal packing effects for the C3d-CR2(CCP1-2) complex and to study the energetics of the C3d-CR2(CCP1-2) association. The MD simulation suggests a tendency for intermodular twisting in CR2(CCP1-2). We propose a two-step model for recognition and binding of C3d with CR2(CCP1-2), driven by long and short/medium-range electrostatic interactions. We have calculated the matrix of specific short/medium-range pairwise electrostatic free energies of interaction involved in binding and in intermodular communications. Electrostatic interactions may mediate allosteric effects important for C3d-CR2(CCP1-2) association. We present calculations for the pH and ionic strength-dependence of C3d-CR2(CCP1-2) ionization free energies, which are in overall agreement with experimental binding data. We show how comparison of the calculated and experimental data allows for the decomposition of the contributions of electrostatic from other effects in association. We critically compare predicted stabilities for several mutants of the C3d-CR2(CCP1-2) complex with the available experimental data for binding ability. Finally, we propose that CR2(CCP1-2) is capable of assuming a large array of intermodular topologies, ranging from closed V-shaped to open linear states, with similar recognition properties for C3d, but we cannot exclude an additional contact site with C3d.