In Ustilago maydis, cAMP signalling is crucial for successful infection of maize plants. Strains are non-pathogenic if mutated in any of the currently identified components of this signalling pathway, such as the alpha-subunit of a heterotrimeric G protein Gpa3, the adenylate cyclase Uac1 and the regulatory and catalytic subunit of protein kinase A Ubc1 and Adr1 respectively. Deletion of gpa3, uac1 or adr1 triggers filamentous growth, and certain point mutations in gpa3 and ubc1 that mimic a high cAMP level display a glossy colony phenotype. Screening an autonomously replicating U. maydis library in such a background (gpa3Q206L), we identified sql1 as a suppressor of the glossy colony phenotype. Interestingly, only alleles carrying C-terminal truncations of Sql1 were able to complement the mutant phenotype, suggesting a gain-of-function by these variants. Sql1 is a functional homologue of the yeast transcriptional repressor Ssn6p and contains 10 tetratricopeptide repeats (TPRs), of which the first six are important for suppressor function. Truncated sql1 alleles that suppress the glossy colony phenotype of gpa3Q206L strains induce filamentous growth when introduced in wild type. Filamentation of these strains is reversed in the presence of cAMP. We present a model in which Sql1 is part of an evolutionary conserved Sql1-Tup1 transcriptional repressor complex that antagonizes cAMP signalling by repressing cAMP-regulated genes.