Small RNAs (sRNAs) are critical regulators of gene expression in bacteria, but we lack a clear understanding of how new sRNAs originate and get integrated into regulatory networks. A major obstacle to elucidating their evolution is the difficulty in tracing sRNAs across large phylogenetic distances. To overcome this roadblock, we investigated the prevalence of sRNAs in more than a thousand genomes across Enterobacterales, a bacterial order with a rare confluence of factors that allows robust genome-scale sRNA analyses: several well-studied organisms with fairly conserved genome structures, an established phylogeny, and substantial nucleotide diversity within a narrow evolutionary space. Using a covariance modeling-based approach, we analyzed the presence of hundreds of sRNAs and discovered that a majority of sRNAs arose recently, and uncovered protein-coding genes as a potential source for the generation of new sRNA genes. A detailed investigation of the emergence of OxyS, a peroxide-responding sRNA, demonstrated that it evolved from a fragment of a peroxidase mRNA. Collectively, our data show that the erosion of protein-coding genes can result in the formation of new sRNAs that continue to be part of the original regulon. This novel insight provides a fresh framework for understanding how new sRNAs originate and get incorporated into preexisting regulatory networks.