The context-dependent nature of plant-microbe interaction in the rhizosphere is of significance in terms of the consistency of beneficial microbe effects in inoculated plants. We performed a series of experiments testing the effect of inoculation with arbuscular mycorrhizal fungi (AMF) and a root-associated fungus, Penicillium pinophilum EU0013, on the growth and root colonization of tomato and lettuce. Three AMF species (Rhizophagus irregularis, Rhizophagus intraradices, and Claroideoglomus etunicatum) and Penicillium (inoculum from corn and wheat media) were used in AMF-plant, Penicillium-plant, and AMF-Penicillium-plant partnerships. In lettuce, we also tested C. etunicatum interaction with Penicillium under different soils (river sand, commercial soil, and river sand + commercial soil). Penicillium pinophilum EU0013 showed phosphate solubilization, siderophore and organic acid production traits in in-vitro assays. In tomato and lettuce, mycorrhizal and Penicillium root colonization were increased during co-inoculation compared to single AMF or Penicillium treatment, indicating that a reciprocal fungal stimulation occurred during AMF-endophyte interaction in both hosts. In tomato, the inoculation with only Penicillium (from wheat medium) or in combination with AMF, significantly improved host weights. In lettuce, fresh weight was significantly improved when Penicillium from corn medium was used in combination with C. etunicatum. However, when the same AMF-Penicillium consortium was tested using Penicillium from wheat media, co-infection stress in the form of retarded growth, wilting of leaves and mortality occurred, depending on the soil. The pattern of negative effects could be rapid and transient, where wilting, slow growth, mortality, and recovery occurred (in river sand), or gradual and persistent where there was slower growth but no mortality (as in commercial and mixed soil). Target host, soil, culture media of inoculum and fungal consortium composition are important considerations in the exploitation of AMF and Penicillium pinophilum EU0013 for improving vegetable growth.