To overcome phosphorus (P) deficiency, about 80% of plant species establish symbiosis with arbuscular mycorrhizal fungi (AMF), which in return constitute a major sink of photosynthates. Information on whether plant carbon (C) allocation towards AMF increases with declining availability of the P source is limited. We offered orthophosphate (OP), apatite (AP), or phytic acid (PA) as the only P source available to arbuscular mycorrhiza (AM) (Solanum lycopersicum x Rhizophagus irregularis) in a mesocosm experiment, where the fungi had exclusive access to each P source. After exposure, we determined P contents in the plant, related these to the overall C budget of the system, including the organic C (OC) contents, the respired CO2, the phospholipid fatty acid (PLFA) 16:1ω5c (extraradical mycelium), and the neutral fatty acid (NLFA) 16:1ω5c (energy storage) at the fungal compartment. Arbuscular mycorrhizal (AM) plants incorporated P derived from the three P sources through the mycorrhizal pathway, but did this with differing C-P trading costs. The mobilization of PA and AP by the AM plant entailed larger mycelium infrastructure and significantly larger respiratory losses of CO2, in comparison with the utilization of the readily soluble OP. Our study thus suggests that AM plants invest larger C amounts into their fungal partners at lower P availability. This larger C flux to the AM fungi might also lead to larger soil organic C contents, in the course of forming larger AM biomass under P-limiting conditions. © 2020, The Author(s).