The use of grasses such as ryegrass and fescues infected with endophytic fungi of the Epichloë genus is widespread in New Zealand’s pastoral systems. Each endophyte–cultivar combination represents a distinctive genome–genome association, resulting in unique biological outcomes. The wider influence of these interactions on rhizosphere microbiology are not well characterised. This is important, because there may be opportunities or risks associated with selective disruption of the rhizosphere microbiota. We explored the interaction of two commercially used endophyte fungi, E. festucae var. lolii strains AR1 and AR37, within a genetically uniform breeding line of perennial ryegrass (Lolium perenne cv. Samson 11104) on the rhizosphere metabolome and the composition of the fungal, bacterial, and Pseudomonas communities. There were strong differences in the rhizosphere metabolomes between infested and non-infested ryegrass strains (P = 0.06). These were attributed to shifts in various n-alkane hydrocarbon compounds. The endophyte-associated alteration in rhizosphere metabolome was linked to changes in the total bacterial (P < 0.01) and fungal (P < 0.05) rhizosphere communities. Furthermore, there was varying levels of support for endophyte-specific (AR1 v. AR37) impacts on the bacterial and fungal communities. Pseudomonas bacterial communities were not influenced by endophyte infection of ryegrass (P = 0.834).