Silicon is the second most abundant element in the Earth’s crust. Plants acquire silicon entirely though root uptake and can accumulate up to 10% of dry mass in silicon, more than any other macronutrient. While not considered an essential nutrient, silicon has been shown to play important functional roles in the alleviation of biotic (e.g. insect herbivores) and abiotic (e.g. drought) stresses. Plant roots host a number of mutualistic microbes, including arbusucular mycorrhizal fungi (AMF) and nitrogen fixing Rhizobium bacteria (NFB), but little is known about how these microbial partners affect silicon uptake. Here we show how AMF can promote silicon uptake in sugarcane (Saccharum spp.), especially when levels of bioavailable silicon in the soil are low. Increasing silicon accumulation resulted in increased plant growth, enhanced rates of photosynthesis and crucially increased resistance to a root-feeding insect pest (Dermolepida albohirtum). In particular, silicon reduced root herbivore growth rates by 107% and 81% in plants inoculated with two communities of AMF. Moreover, there was a negative relationship between levels of phenolic-based chemical defences and silicon concentrations, potentially indicative of a defensive trade-off. We suggest this may be why a number of root-feeding insects counterintuitively perform better on phenolic-rich plants. Working with lucerne (Medicago sativa), we present initial results showing how silicon supplementation promoted root nodulation (+44%) and NFB activity. Silicon indirectly stimulated biosynthesis of essential amino acids which became significantly more concentrated in the foliage of silicon-supplemented plants. This caused a small, but significant, increase in aphid (Acyrthosiphon pisum) abundance aboveground. We conclude that the beneficial effects of silicon accumulation in plants can be enhanced by AMF and silicon accumulation has positive impacts on NFB activity.