With the increasing availability of high-quality fungal genomes, effectors conserved among species and genera have been uncovered. Two avirulence effectors, AvrLm10A and AvrLm10B, of Leptosphaeria maculans, responsible for stem canker of oilseed rape, are members of such a large family of conserved effectors. AvrLm10A and AvrLm10B are neighboring genes in divergent transcriptional orientation. Sequence searches within the L. maculans genome showed that AvrLm10A/AvrLm10B belong to a multigene family comprising five pairs of genes with similar tail-to-tail organization, specifically expressed during biotrophic stages of infection. Two of the corresponding protein pairs, including AvrLm10A and AvrLm10B, have the ability to physically interact. AvrLm10A homologues were identified in more than 30 Dothideomycete and Sordariomycete plant-pathogenic fungi. One of them, SIX5, is an effector from Fusarium oxysporum f.sp. lycopersici (Fol) physically interacting with the avirulence effector Avr2 and required for the movement of Avr2 from cell- to-cell through plasmodesmata. We demonstrated that members of the AvrLm10A family in L. maculans can complement SIX5 function in plant cell-to-cell mobility assays and Fol virulence. We found that AvrLm10A/SIX5 homologues were associated with at least eight distinct effector families, suggesting an ability to cooperate with different effectors. These results point to a general role of the AvrLm10A/SIX5 proteins as “cooperator proteins”