Echinococcus multilocularis is the most important food-borne parasite in Europe. Its natural definitive host is red fox while other canid species play a secondary role in the maintenance of its endemics. However, recent studies call attention to the potential of golden jackal (Canis aureus) as a suitable definitive host for E. multilocularis. Our study aimed to evaluate the egg production ability, as an indicator of reproductive success, of E. multilocularis adults in different hosts and crowding conditions. With investigation of 111 and 82 parasites from 33 red foxes and 29 golden jackals, respectively, this study ascertained that the proportion of worms with mature eggs were significantly lower in golden jackals than in red foxes. Those worms, which produced mature eggs in golden jackal hosts, originated from less crowded infrapopulations than their fox-originated counterparts. Other characteristics of parasitism, such as mean intensity, fertile worm count, and mean egg production were similar in the two hosts. Comparing these findings to evolutionary data on different canid taxa, we hypothesised that mutual presence of red fox and a differently evolved host of E. multilocularis might contribute to the formation of stable parasite circulation in these multi-host systems.