Although the RNA polymerase (Pol) II machinery inherently initiates transcription in one direction, promoter regions are often “bidirectional” in vivo, giving rise to divergent RNA transcripts, many of which are non-coding and highly unstable. Here, we use a functional evolutionary approach to address whether bidirectional promoter regions are a mechanistic consequence of Pol II transcription or serve an evolved biological function. This involves nascent transcript mapping in S. cerevisiae strains containing large segments of foreign, and hence evolutionarily irrelevant, yeast DNA. Promoter regions in foreign species environments lose the directionality they have in their native species, indicating that DNA sequences and proteins co-evolve to promote directional transcription. Furthermore, fortuitous promoters emerge frequently in foreign DNA, and these produce equal transcription in both directions. Thus, without evolutionary pressure, the transcriptional ground state of promoter regions is intrinsically bidirectional. Interestingly, promoter regions of newly evolved genes tend to promote bidirectional transcription, and when fortuitous promoters arise in evolution, transcription factor binding sites are either purged through mutation or retained to enable new functionality. These results indicate that promoter regions are intrinsically bidirectional and are shaped by evolution to bias transcription of coding transcripts while suppressing non-coding transcriptional noise. Overall design: We transferred artificial chromosomes made of DNA extracted from K. lactis and D. hansenii to S. cerevisiae and performed NET-Seq