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Filamentous growth is one of the key features of pathogenic fungi during the early infectious phase. The pseudohyphal development of yeastSaccharomyces cerevisiaeshares similar characteristics with hyphae elongation in pathogenic fungi. The expression ofFLO11is essential for adhesive growth and filament formation in yeast and is governed by a multilayered transcriptional network. Here we discovered a role for the histone acetyltransferase general control nonderepressible 5 (Gcn5) in regulatingFLO11-mediated pseudohyphal growth. The expression patterns ofFLO11were distinct in haploid and diploid yeast under amino acid starvation induced by 3-amino-1,2,4-triazole (3AT). In diploids,FLO11expression was substantially induced at a very early stage of pseudohyphal development and decreased quickly, but in haploids, it was gradually induced. Furthermore, the transcription factor Gcn4 was recruited to the Sfl1-Flo8 toggle sites at theFLO11promoter under 3AT treatment. Moreover, the histone acetylase activity of Gcn5 was required forFLO11induction. Finally, Gcn5 functioned as a negative regulator of the noncoding RNAICR1, which is known to suppressFLO11expression. Gcn5 plays an important role in the regulatory network ofFLO11expression via Gcn4 by downregulatingICR1expression, which derepressesFLO11for promoting pseudohyphal development.