The expansion of marine aquaculture production is driven by a high market demand for marine proteins and a stagnation of wild catch of fish. Bivalve farming, i.e., the cultivation of oysters, mussels and scallops, is an important part of the ongoing market dynamics and production expansion. As marine spatial planning is considering various use purposes, available space for near-shore aquaculture is already becoming scarce; this has fueled research and development initiatives to enable production installations further offshore. The highly energetic conditions at more exposed offshore marine sites lead to increased loads on aquaculture systems and their components and it is still not sufficiently understood how the load transfer from oceanic environmental conditions onto shellfish-encrusted surfaces attached to elastic ropes may be appropriately quantified. This study data gathered large-scale data sets in a wave tank facility, which are used to validate a novel, numerical model, building on the dynamics of rope structures which allows for the determination of the hydrodynamic loads transferred to the dropper lines. The forces and hydrodynamic parameters are measured and numerically analyzed. Based on the results, drag and inertia coefficients are determined. A drag coefficient of CD = 1.1 and an inertia coefficient of CM = 1.7 are recommended to model shellfish-encrusted dropper lines exposed to oscillatory flows with KC = 40–90. The numerical model for the determination of wave-induced forces on mussel dropper lines is developed and validated using the experimental data. It employs a modified Morison equation, which takes into account the displacement of the mussel dropper line. The influence of varying aquaculture-related parameters is discussed by applying the numerical model. Based on the gathered insights, recommendations can be given from an engineering point of view concerning the optimal placement of mussel aquaculture within the water column.