Arbuscular mycorrhizal fungi (AMF) facilitate plant uptake of mineral nutrients, particularly phosphorus, and draw organic carbon from the plant. The ability of symbiotic AMF to utilize external non-symbiotic carbon sources remains unclear, complicating our comprehension of their ecosystem functions. Here we examine the direct absorption of exogenous 13C1-labeled myristate by symbiotic AMF and their growth responses using an in-vitro dual culture system. We also investigated the impact of exogenous myristate on the carbon‒phosphorus exchange between AMF and two different host plants in a greenhouse experiment, employing both stable isotope labeling (13CO2) and profiling of P transporter genes. Our results indicate that the extraradical hyphae of symbiotic AMF are capable of absorbing external myristate and transporting it (or its metabolic products) to intraradical structures. Myristate serves a dual function as a carbon source and signaling molecule, leading to increased intraradical and extraradical fungal biomasses, with RNA-Seq data indicating a suppressed mycorrhizal defense response as a potential mechanism. Intriguingly, exogenous myristate generally reduced the mycorrhizal phosphorus benefits for both alfalfa and rice, and decreased their carbon allocation to symbiotic AMF, likely by interfering with their normal trading mechanisms. These findings provide novel insights into the ecosystem functions and ecological applications of AMF.