Investigating how arbuscular mycorrhizal fungi (AMF)-plant interactions vary with edaphic conditions provides an opportunity to test the context-dependency of interspecific interactions. The relationship between AMF and their host plants in the context of other soil microbes was studied along a gradient of heavy metal contamination originating at the site of zinc smelters that operated for a century. The site is currently under restoration. Native C3 grasses have reestablished, and C4 grasses native to the region but not the site were introduced. Interactions involving the native mycorrhizal fungi, non-mycorrhizal soil microbes, soil, one C3 grass (Deschampsia flexuosa), and one C4 grass (Sorghastrum nutans) were investigated using soils from the two extremes of the contamination gradient in a full factorial greenhouse experiment. After 12 weeks, plant biomass and root colonization by AMF and non-mycorrhizal microbes were measured. Plants from both species grew much larger in soil from low-contaminated (LC) origin than high-contaminated (HC) origin. For S. nutans, the addition of a non-AMF soil microbial wash of either origin increased the efficacy of AMF from LC soils but decreased the efficacy of AMF from HC soils in promoting plant growth. Furthermore, there was high mortality of S. nutans in HC soil, where plants with AMF from HC died sooner. For D. flexuosa, plant biomass did not vary with AMF source or the microbial wash treatment or their interaction. While AMF origin did not affect root colonization of D. flexuosa by AMF, the presence and origin of AMF did affect the number of non-mycorrhizal (NMF) morphotypes and NMF root colonization. Adding non-AMF soil biota reduced Zn concentrations in shoots of D. flexuosa. Thus the non-AMF biotic context affected heavy metal sequestration and associated NMF in D. flexuosa, and it interacted with AMF to affect plant biomass in S. nutans. Our results should be useful for improving our basic ecological understanding of the context-dependency of plant-soil interactions and are potentially important in restoration of heavy-metal-contaminated sites.