Major mechanisms of azole resistance in Aspergillus fumigatus involve overexpression of the azole target protein encoded by cyp51A. The elevated expression originates from the duplication of an enhancer element in its promoter, serving as a binding platform for AtrR and SrbA, two central transcription factors that orchestrate the activation of ergosterol biosynthesis genes and azole resistance. Alongside AtrR and SrbA, several other transcription factors were shown to be crucial to mediate azole tolerance. Here, we unveil RttA as a further protein involved in the regulation of ergosterol biosynthesis and azole resistance in A. fumigatus. Because the gene was wrongly annotated, its encoded protein remained a protein with unclear function. Based on mapped RNA-seq reads, the coding sequence was corrected, yielding a DNA-binding protein comprising a Zn₂Cys₆ binuclear zinc cluster. Domain analysis and structural comparisons implied similarity between RttA and Neurospora crassa NcSR and yeast Upc2, both involved in sterol regulation and azole resistance. Through deletion and overexpression of rttA, we confirm its role in azole resistance. Transcriptional profiling of atrR, srbA, and rttA deletion mutants revealed that rttA expression depends on both AtrR and SrbA. In addition, our analyses uncovered a positive regulatory role for RttA in the expression of efflux pump-encoding genes and sterol homeostasis through activation of erg6 expression. In agreement, the lack of rttA led to a substantial accumulation of the Erg6 substrate lanosterol. Collectively, this work elucidates RttA as a transcription factor in the clinically important fungal pathogen A. fumigatus involved in the regulation of ergosterol biosynthesis and azole tolerance.