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R2 retrotransposons reside exclusively within the 28S regions of 10–20% of all rDNA genes comprising the nucleolar organizer loci on the X and Y chromosomes of Drosophila melanogaster. These R2-inserted genes are normally silent and heterochromatic. When expressed, however, the R2 transcript is co-transcribed with the 28S rRNA. Self-cleavage releases a 3.6 kb mature R2 transcript that encodes a single protein with endonuclease and reverse transcriptase activities that facilitate R2 element transposition by target-primed reverse transcription. While we know the molecular details of R2 transposition, we know little about the genetic mechanisms that initiate R2 transcription. Here, we examine R2 expression in wild type versus mutant backgrounds. R2 expression in stage 1–4 wild type egg chambers was variable depending on the stock. R2 expression was silent in wild type stages 5–10 but was consistently active during nurse cell nuclear breakdown in stages 12–13 regardless of the genetic background. Massive R2 expression occurred in stages 5–10 upon loss of Udd, an RNA Pol I transcription factor. Similarly, loss of Nopp140, an early ribosome assembly factor, induced R2 expression more so in somatic tissues. Interestingly, over-expression of the Nopp140-RGG isoform but not the Nopp140-True isoform induced R2 expression in larval somatic tissues, suggesting Nopp140-RGG could potentially affect rDNA chromatin structure. Conversely, Minute mutations in genes encoding ribosomal proteins had minor positive effects on R2 expression. We conclude that R2 expression is largely controlled by factors regulating RNA Pol I transcription and early ribosome assembly.