In cleaning symbioses, colonization of hosts by parasites and other epibionts often varies across habitats, and this variability could influence the net effect of cleaners on host fitness. We investigated how variation in environmental fouling (i.e., epibiont colonization and accumulation of particulate matter) influenced symbiont populations and partner regulation in a crayfish–branchiobdellidan worm cleaning symbiosis. We manipulated initial worm density and environmental fouling in a laboratory experiment. We monitored the number of worms (both stocked, large worms and juvenile worms born during the experiment) and the number of worm cocoons deposited on the crayfish for 8 wk. Initial worm density and fouling potential of the environment significantly affected removal of large worms by crayfish. Loss of large worms was higher in the high-initial-density and the low-fouling treatments during the 1^st wk of the experiment, after which the density of large worm numbers did not differ among treatments. Cocoon production did not differ among treatments, but cocoon production ceased early in the low-fouling treatment with high initial densities. Number of juvenile worms was higher in the high- than in the low-fouling treatments by the end of the experiment, probably because of increased availability of epibiotic resources. Fouling treatment had a greater effect on total branchiobdellidan population size (initial worms plus juveniles) than did initial worm density. These results demonstrate that initial symbiont density and environmental context can influence partner regulation by the host and cleaner reproduction and abundance in a cleaning symbiosis.