The large amount of genomic sequence data has enabled the discovery of many noncoding nucleic acid structures involved in numerous cellular and physiological processes. The boxC motif is a remarkably conserved, small, and pervasive element in bacteria that was first reported in the late 1980s. Although the motif has been independently discovered by multiple research groups, its structure and biological role(s) have remained obscure. We developed a computational pipeline to identify more than unique 18,000 boxC elements in all classes of bacteria and analyze their distribution within genomes. The motif is most commonly found downstream of the 3’-ends of coding regions. Most individual genomes contain up to 20 copies, but some have more than 500. Bioinformatic analysis reveals that the DNA has the potential to fold into a unique and conserved tertiary structure, supported by biochemical experiments. The prevalence of boxC in bacterial genomes and its distinctive structure suggest it has an important cellular function. Similar to boxC, there are many more enigmatic structured DNA and RNA elements. The methodology used in our study can be applied to the analysis of many additional motifs to broaden our understanding of the roles of noncoding regions of bacterial genomes.