The mechanisms by which gene expression patterns emerge during evolution are poorly understood. The sea urchin spec genes offer a useful means to investigate evolutionary mechanisms. Genes of the spec family from Strongylocentrotus purpuratus and Lytechinus pictus have identical patterns of aboral ectoderm-specific expression but exhibit species-specific differences in copy number, genomic structure, temporal expression, and cis-regulatory architecture. Here, we identify spec genes from a phylogenetic intermediate, Strongylocentrotus franciscanus, to gain insight into the evolution of the spec gene family and its transcriptional regulation. We identified two spec genes in the S. franciscanus genome, sfspec1a and sfspec1b, that were orthologous to spec1 from S. purpuratus. sfspec1b transcripts began to accumulate at the blastula stage and became progressively more abundant; this was reminiscent of spec expression in L. pictus but different from that in S. purpuratus. As expected, sfspec1b expression was restricted to aboral ectoderm cells. The six-exon structure of the sfspec1b genomic locus was identical to that of the S. purpuratus spec genes and was bounded by two repeat-spacer-repeat (RSR) repetitive sequence elements, which are conserved features of S. purpuratus spec genes and function as transcriptional enhancers. The enhancer activity of the sfspec1b RSRs was comparable to that of their S. purpuratus counterparts, although the placement and orientation of crucial cis-regulatory elements within the RSRs differed. We discovered a spec gene in S. franciscanus that was only distantly related to other spec genes but was highly conserved in S. purpuratus. Unexpectedly, this gene was expressed exclusively in endoderm lineages. Our results show that the evolution of spec cis-regulatory elements is highly dynamic and that substantial alterations can occur when maintaining or grossly modifying gene expression patterns.