Gene duplications and transcriptional enhancer emergence/modifications are thought having greatly contributed to phenotypic innovations during animal evolution. Nevertheless, little is known about how enhancers evolve after gene duplication and how regulatory information is rewired between duplicated genes. The Drosophila melanogaster bric-a-brac (bab) complex, comprising the tandem paralogous genes bab1 and bab2, provides a paradigm to address these issues. We previously characterized an intergenic enhancer (named LAE) regulating bab2 expression in the developing legs. We show here that bab2 regulators binding directly the LAE also govern bab1 expression in tarsal cells. LAE excision by CRISPR/Cas9-mediated genome editing reveals that this enhancer appears involved but not strictly required for bab1 and bab2 co-expression in leg tissues. Instead, the LAE enhancer is critical for paralog-specific bab2 expression along the proximo-distal leg axis. Chromatin features and phenotypic rescue experiments indicate that LAE functions partly redundantly with leg-specific regulatory information overlapping the bab1 transcription unit. Phylogenomics analyses indicate that (i) the bab complex originates from duplication of an ancestral singleton gene early on within the Cyclorrhapha dipteran sublineage, and (ii) LAE sequences have been evolutionarily-fixed early on within the Brachycera suborder thus predating the gene duplication event. This work provides new insights on enhancers, particularly about their emergence, maintenance and functional diversification during evolution. Author summary: During animal evolution, de novo emergence and rewiring of transcriptional enhancers have contributed to morphological innovations. However, how enhancers regulate distinctly gene duplicates and are evolutionary-fixed remain largely unknown. The Drosophila bric-a-brac (bab) locus, comprising the tandemly-duplicated genes bab1 and bab2, provides a good paradigm to address these issues. In this study, genetic analyses show a partial co-regulation of both genes in the developing leg depending on tissue-specific transcription factors known to bind an intergenic enhancer. Genome editing reveals that this enhancer is shared by both genes and is also critically required for bab2-specific expression. Chromatin features and phenotypic rescue experiments indicate the existence of partly-redundant limb-specific regulatory information within the bab1 transcription unit. Phylogenomics analyses among Diptera indicate that the Drosophila bab locus originates from duplication of a singleton gene within the Brachycera lineage. Lastly, we show that whereas bab1 promoter and leg enhancer sequences have been well conserved after the duplication event, bab2 promoter and other bab enhancers have evolved more recently in the Cyclorrhapha sublineage. This work brings some new insights about (i) how a single enhancer can drive specificity among tandem gene duplicates, and (ii) how enhancers evolutionary adapt with distinct cognate gene promoters. [ABSTRACT FROM AUTHOR]