Despite recent findings that mutualistic interactions between two species may be greatly affected by species external to the mutualism, the implications of such multi–species interactions for the population dynamics of the mutualists are virtually unexplored. In this paper, we ask how the mutualism between the shoot–base boring weevil Apion onopordi and the rust fungus Puccinia punctiformis is influenced by the dynamics of their shared host plant Cirsium arvense, and vice versa. In particular, we hypothesized that the distribution of the weevil's egg load between healthy and rust–infected thistles may regulate the abundance of the mutualists and their host plant. In contrast to our expectations we found that the dynamics of the mutualists are largely determined by the dynamics of their host. This is, to our knowledge, the first demonstration that the dynamics of a mutualism are driven by a third, non–mutualistic species.