Ribosome biogenesis drives cell growth and requires a huge expenditure of cellular resources. In S. cerevisiae, the ribosomal proteins (RP) are encoded by 138 genes (RPGs), although exactly how the RPG transcription factors (TFs) Rap1, Fhl1 and Ifh1 function in the tight co-regulation of RPG transcription is not well understood. In this work, we define two categories of RPG promoters, differentiated by the additional binding of the HMG-B protein Hmo1. The two promoter categories show distinct differences in TF binding location, and in the recruitment of Fhl1. We have also identified the presence of dynamic (“fragile”) nucleosomes in RPG promoters, which coincide with sites of TF binding. Our investigations into the RPG activator protein Ifh1 revealed that its Gcn5-dependent acetylation dampens activation. We further show that two pathways help regulate Ifh1 promoter binding, one involving pre-rRNA processing proteins, the other involving the TORC1 downstream effector kinase, Sch9.