Rice roots engage in symbiosis with ancient symbiotic fungi such as R. irregularis, whilst resisting invasion of the detrimental fungus M. oryzae, a major causative agent of the rice blast (leaf) disease. M. oryzae can also invade rice roots with simple non-melanised hyphopodia formed on the rice root surface, very similar to R. irregularis. This similarity in behaviour has raised questions whether the biotrophic pathogen adopts an endophytic lifestyle during rice root colonisation, possibly as a disguise to bypass the plant defence machinery whilst entering the host. Identifying shared plant genes and development programmes utilised by M. oryzae and R. irregularis during rice root invasion will provide a better understanding of how the host plant responds to and accommodates both fungi in its root. The work presented here, describes a novel function of three Oryza sativa plasma membrane receptors (Chitin Elicitor Receptor Kinase 1, CERK1; Nod Factor Receptor 5, NFR5 and Chitin Elicitor Binding Protein, CEBiP) in enabling M. oryzae invasion of rice roots. It also demonstrates, for the first time, a role of OsNFR5 as a compatibility factor, rather than a defence receptor during M. oryzae rice leaf infection. Unexpectedly, OsCEBiP was found to be involved in rice root colonisation by R. irregularis, challenging existing reports while presenting a different perspective on the possible co-functioning of the LysM-RLP with OsCERK1 during AM symbiosis. Excitingly, OsCERK1 emerged as a common co-receptor for AM symbiosis, immunity signalling and rice root invasion by M. oryzae, supporting a diverse role of the LysM-RLK in the perception of an array of signalling molecules. Lastly, transcriptome comparison analysis performed in this study revealed a new set of co-induced rice genes (Exo70-H3b exocyst, Lectin Receptor-Like Kinase, LecRLK and DUF538 genes encoding ‘proteins of unknown function) that may be commonly required for the invasion of rice roots by both symbiotic and detrimental fungi. These findings lend strong support to the long-standing hypothesis that plant pathogens exploit genetic pathways established in the ancient arbuscular mycorrhizal symbiosis to facilitate their invasion of the host plant. They also have significant implications for effective crop improvement and disease control strategies, which will contribute to global food security.