Enterobacterial repetitive intergenic consensus (ERIC) sequence is a transcription-modulating, nonautonomous, miniature inverted-repeat transposable element. Its origin and the mechanism of highly varying incidences, limited to Enterobacteriaceae and Vibrionaceae, have not been identified. In this study, distribution and divergence of ERICs along bacterial taxonomic units were analyzed. ERICs were found among five families of gammaproteobacteria, with the copy numbers varying with exponential increments. The variability was explained by genus (45%) and species (36%) affiliations, indicating that copy numbers are specific to subfamily taxa. ERICs were interspersed in genomes with considerable divergences. Locations of ERICs in a genome appeared to be strongly conserved in a strain, moderately in a species or a genus, and weakly in a family. ERICs in different species of a genus were from the identical population of sequences while ERICs in different genera of a family were nearly identical. However, ERICs in different families formed distinct monophylectic groups, implying vertical transmission of diverging population of sequences. In spite of large difference in copy numbers, overall intra-genome evolutionary distances among ERICs were similar among different species, except for a few genomes. The exceptions substantiated hypotheses of genetic drifts and horizontal gene transfers of mobility capacity. Therefore, the confined, variable distribution of ERIC could be explained as a two-step evolution: introduction and proliferation of ERIC in one of the progenitors of gammaproteobacteria, followed by vertical transmission under negative selection. Deterioration of sequences and reduction in copy number were concluded to be the predominant patterns in the evolution of ERIC loci.