The fungal pathogen Rhizoctonia solani AG8 causes substantial losses to cereal and legume production in Australia and the Pacific Northwest of the United States of America. Mutant analyses have revealed a critical role for ethylene mediated defence signalling for resistance to R. solani AG8 in the model legume Medicago truncatula which is, at least in part, mediated by ethylene dependent accumulation of isoflavonoids. In this study we investigate the potential for members of the ethylene response transcription factor (ERF) family in mediating the isoflavonoid and defence response. A strong and early Rhizoctonia-responsive expression pattern was observed for many of the class IX ERFs in the moderately resistant wild type line A17, while the ethylene insensitive and highly susceptible mutant sickle (skl) showed a very limited regulation of this class. Conversely, the skl mutant demonstrated up-regulation of class II ERFs known to act as transcriptional repressors. Analysis of the presence of the GCC box promoter element, thought to be responsible for ERF binding and transcriptional activity, in genes differentially regulated in A17 suggests indirect or alternative mechanisms of ERF mediated gene regulation may be contributing to the large scale transcriptional adaptation of A17 following R. solani AG8 infection. Comparison of the expression profile with that following infection of A17 and skl with the symbiotic bacterium Sinorhizobium medicae suggests that legumes have adapted the ERF family to perform diverse roles to balance defence against pathogens and symbiosis with beneficial microorganisms in the same root tissue.