Plant pathogens secrete proteins, known as effectors, that function in the apoplast and inside plant cells to promote virulence. Despite their importance, our understanding of fungal effector function and detection by immunity receptors remains poor. Using protein x-ray crystallography, we identify a new structural class of effectors hidden within the secreted in xylem (SIX) effectors from Fusarium oxysporum f. sp. lycopersici (Fol). The recognised effectors, Avr1 (SIX4) and Avr3 (SIX1), represent the founding members of the Fol dual-domain (FOLD) effector class. We show that Avr1 and Avr3 are recognised by the resistance proteins, I and I-3, respectively using a protein-mediated phenotyping approach. Utilising a structurally guided mutagenesis approach, we identify residues in Avr1 that are crucial for recognition by the I resistance protein. We also determine the recognition specificity of the I resistance protein is dictated by the island domain, with a single amino acid mutation capable of rescuing recognition in an allelic variant of I that cannot recognise Avr1. Collectively, these data will aid future studies to understand the molecular basis of F. oxysporum effector function and recognition, and by extension, the design and engineering of immunity receptors with novel recognition specificities to help protect plants against Fusarium wilt disease.