Current viral docking models have relied upon the assumption that bond formation and breakage are independent of viral and docking surface geometry, as well as the forces exerted on the bonds. This assumption, known as the equivalent site hypothesis (ESH), is examined in detail using a newly developed simulation technique—Brownian adhesive dynamics (BRAD). The simulation couples the thermal motion of viral particles with adhesive dynamics models to characterize the effect of bonding on viral motion. We use the binding of HIV-like particles to CD4 expressing cells as a model system to illustrate the utility of BRAD. Comparison of the transition rates between bound states predicted by ESH and the rates resulting from BRAD simulations show dramatic differences; at values of the equilibrium crosslinking constant, KxRT, where ESH suggests all virus adhesion proteins will be bound (KxRT = 106), BRAD predicts not all virus adhesion proteins will be bound. At values of the equilibrium crosslinking constant used in typical ESH calculations of virus docking (KxRT = 1) we find BRAD simulations predict no binding. The mean bond density from BRAD models is often much lower than that predicted by ESH for equivalent parameter values. BRAD suggests that the viruses are much less well bound than ESH predicts. The differences suggest that binding models for viruses need to be reexamined closely. BRAD is a simulation technique that will be useful for quantifying the receptor-mediated binding of a wide variety of viruses to cells.