Maf1 is a putative repressor of RNA polymerase (pol) III transcription that is conserved from yeast to humans. Here we show that Maf1 is a common component of multiple signaling pathways in S. cerevesiae that sense changes in the cellular environment and repress pol III transcription. Signaling pathways activated in response to rapamycin-induced nutrient limitation, DNA damage, and secretory pathway defects all require Maf1 in order to affect pol III transcriptional repression. In addition, Maf1 was required for repression of pol III transcription during the normal yeast growth cycle. Biochemical studies identified the initiation factor TFIIIB as a target of Maf1-dependent repression and revealed a defect in TFIIIB-DNA complex assembly under repressing conditions.