Host monopolization theory predicts symbiotic organisms inhabiting morphologically simple, relatively small and scarce hosts to live solitarily as a result of territorial behaviors. We tested this prediction with Tunicotheres moseri, an endosymbiotic crab dwelling in the atrial chamber of the morphologically simple, small, and relatively scarce ascidian Styela plicata. As predicted, natural populations of T. moseri inhabit ascidian hosts solitarily with greater frequency than expected by chance alone. Furthermore, laboratory experiments demonstrated that intruder crabs take significantly longer to colonize previously infected compared to uninfected hosts, indicating as expected, that resident crabs exhibit monopolization behaviors. While territoriality does occur, agonistic behaviors employed by T. moseri do not mirror the overt behaviors commonly reported for other territorial crustaceans. Documented double and triple cohabitations in the field coupled with laboratory observations demonstrating the almost invariable success of intruder crabs colonizing occupied hosts, suggest that territoriality is ineffective in completely explaining the solitary social habit of this species. Additional experiments showed that T. moseri juveniles and adults, when searching for ascidians use chemical cues to avoid hosts occupied by conspecifics. This conspecific avoidance behavior reported herein is a novel strategy most likely employed to preemptively resolve costly territorial conflicts. In general, this study supports predictions central to host monopolization theory, but also implies that alternative behavioral strategies (i.e., conflict avoidance) may be more important than originally thought in explaining the host use pattern of symbiotic organisms.