HIV-1 protease is an essential enzyme in the life cycle of human immunodeficiency virus (HIV) and hence is one of the most important targets for antiviral drug design. Although there are ten FDA approved drugs against HIV protease (PR), their long term usage elicits mutations leading to drug resistance. As a result, novel therapeutic approaches are being explored including synthetic antibodies. Recently, a murine monoclonal antibody, mAB1696 (mAB) was reported to inhibit PR by preventing dimerization. Crystallographic data could reveal only six protease residues that interact with mAB. The present study employs a range of computational techniques, starting from protein-protein docking to all-atomic molecular dynamics simulations to generate plausible 3D structures of PR-mAB complex. Results show that mAB interacts very strongly with several PR dimer interface residues, such as Gln7, Arg8 (N-terminal), Cys95, Leu97 (C-terminal), Thr26, Gly27 (active site), Gly49, Ile50 (flap), apart from its interactions with the PR epitope region, Pro1-Trp6 (N-terminal). These observations support the hypothesis that binding of mAB prevents the dimerization of PR. The interactions and binding conformations identified in this study could form the basis for designing allosteric inhibitors preventing the dimerization of HIV-1 Protease.