The beneficial root-colonizing fungus Colletotrichum tofieldiae (Ct) mediates plant growth promotion (PGP) upon phosphate (Pi) starvation in Arabidopsis thaliana (Arabidopsis). This activity is dependent on the Trp-metabolism of the host, including indole glucosinolate (IG) hydrolysis. Here we show that Ct resolves several Pi starvation-induced molecular processes in the host, one of which is the downregulation of auxin signaling in germ-free plants, which is restored in the presence of the fungus. Using CRISPR/Cas9 genome editing, we generated an Arabidopsis triple mutant lacking three homologous nitrilases (NIT1-3) that are thought to link IG-hydrolysis products with auxin biosynthesis. Retained Ct-induced PGP in nit1;2;3 mutant plants demonstrated that this metabolic connection is dispensable for the beneficial activity of the fungus. This suggests that either there is an alternative metabolic link between IG-hydrolysis products and auxin biosynthesis, or that Ct restores auxin signaling independently of IG metabolism. We show that Ct, similar to pathogenic microorganisms, triggers Arabidopsis immune pathways that rely on IG metabolism as well as salicylic acid and ethylene signaling. Analysis of IG-deficient myb mutants revealed that these metabolites are indeed important for control of in planta Ct growth: however, enhanced Ct biomass does not necessarily negatively correlate with PGP. We show that Pi deficiency enables more efficient colonization of Arabidopsis by Ct, possibly due to the MYC2-mediated repression of ethylene signaling and changes in the constitutive IG composition in roots.