Bacteriophage genomes can be incredibly compact, making them a useful model for exploring highly optimized genome architectures. This compact nature is often achieved through overlapping open reading frames and regulatory elements of adjacent genes. One instance is the genome of the widely used phage M13, in which 9 of the 10 genes are regulated by ribosomal binding sites (RBS) located internal to the 3’ end of the upstream gene. The overlapping functions of this sequence bring into question the tradeoff between optimal RBS sequence identity, which regulates gene expression levels, and optimal C-terminal sequence identity, which dictates protein structure. To investigate this tradeoff, we have created an M13 library containing sequence variants at 7 known internal RBS. Using Phage and Robotics Assisted Near Continuous Evolution (PRANCE), we can evolve this phage library under mutagenic continuous culture conditions maintained by liquid handling automation. The PRANCE platform allows 48 replicate evolving communities to be maintained indefinitely, each encompassing thousands of generations of phage. Using long-read sequencing to track the evolving phage populations over time allows identification of the highest fitness variants and examination of how the initial library evolves to optimize genetic code for dual regulatory and structural functions. Through tracking phage evolution with exceptionally high throughput and resolution, we are well poised to elucidate the evolutionary mechanisms of genome streamlining in phages.