Whether coevolution determines distribution patterns of facultative symbionts among individuals of a host species is an open question. We used theDictyostelium discoideum-Paraburkholderiasystem to investigate the role of host fitness and symbiont transmission in co-occurrence patterns of naturally occurring (native) host-symbiont strain pairs.P. bonnieais able to persistently infectD. discoideumin the lab, yet few wildD. discoideumisolates natively host this symbiont. If native host-symbiont combinations lead to higher fitness for host and symbiont compared to nonnative combinations, we assumed a stronger chance that coevolution had led to their co-occurrence. We approached the factors that influence the fitness consequences of host-symbiont interactions in terms of host defense mechanisms and symbiont virulence mechanisms. Given a specific combination of host and symbiont, variable host resistance and symbiont proliferation lead to variation in symbiont density, while variable host tolerance and symbiont benevolence lead to variation in host fitness relative to symbiont density. We used both vegetative and social stages of the host life cycle to approximate interactions betweenD. discoideumandP. bonniea, when hosts form social groups and symbiont horizontal transmission is facilitated by these social groups. We found no difference in host defense mechanisms between native and nonnative hosts ofP. bonniea, butP. bonnieapossesses variable phenotypes in proliferation and benevolence. More importantly, variation in symbiont benevolence led to increased horizontal transmission of benevolent strains compared to malevolent strains during the social stage of the host life cycle.