Membrane contact sites enable the exchange of metabolites between subcellular compartments and regulate organelle dynamics and positioning. These structures often contain multiple proteins that tether the membranes, establishing the apposition and functionalizing the structure. In this work, we use drug-inducible tethers in vivo to address how different tethers influence each other. We find that the establishment of a region of membrane proximity can recruit tethers, influencing their distribution between different localizations or protein complexes. In addition, restricting the localization of one tether to a subdomain of an organelle causes other tethers to be restricted there. Finally, we show that the mobility of contact site tethers can also be influenced by other tethers of the same interface. Overall, our results show that the presence of other tethers at contact sites is an important determinant of the behavior of tethering proteins. This suggests that contact sites with multiple tethers are controlled by the interplay between specific molecular interactions and the cross-influence of tethers of the same interface.