The Ci-Dll-A and Ci-Dll-B genes of Ciona intestinalis are arranged in a convergently transcribed gene cluster. This genomic arrangement is similar to that of the multiple bigene clusters of the Dlx homologs in vertebrates. Analysis of whole genome sequences showed that linkage to the Hox cluster is conserved with the vertebrate clusters. Phylogenetic analysis supports gene trees consistent with homology of the ascidian and vertebrate Dlx clusters, and in combination with the apparent conservation of genomic arrangement, it is concluded that the ascidian cluster is most likely homologous with the vertebrate clusters. Using whole-mount in situ hybridization, Ci-Dll-B transcripts were detected in all ectodermal lineages through gastrulation. Expression is radically downregulated in the neurula with detectable expression disappearing around the time that Ci-Dll-A expression appears in the anterior ectoderm. By the late tailbud stage Ci-Dll-Atranscripts were detected in the bilateral atrial primordia and persisted in the atrial rudiments to the larval stage, suggesting a role in development of these neural placode-like structures. This non-overlapping expression contradicts a common pattern seen in clustered genes, where as adjacent paralogs have largely overlapping expression domains. Enhancer sharing is often proposed as an explanation for the overlapping expression of gene cluster members. For this case of non-overlapping expression a model is proposed in which repressors acting at different stages override one or more shared enhancers. The enhancer sharing prevents breakup of the cluster while the independent temporal suppressors hide the presence of the shared enhancers.