The trapezoidal ciliated band (CB) of the postgastrular sea urchin embryo surrounds the oral ectoderm, separating it from adjacent embryonic territories. Once differentiated, the CB is composed of densely arranged cells bearing long cilia that endow the larva with locomotion and feeding capability. The spatial pattern from which the CB will arise is first evidenced during pregastrular stages by expression of the pioneer gene onecut. Immediately after gastrulation, the CB consists of four separate regulatory state domains, each of which express a unique set of transcription factors. These are: (1) The oral apical CB, located within the apical neurogenic field; (2) The animal lateral CB, which bilaterally separates the oral from aboral ectoderm; (3) The vegetal lateral CB, which bilaterally serves as signaling centers; and (4) The vegetal oral CB, which delineates the boundary with the underlying endoderm. Remarkably, almost all of the regulatory genes specifically expressed within these domains are down-regulated by interference with Soxb1 expression, implying activation by this factor in common. In this work we show how the boundaries of the CB subdomains are established, and thus ascertain the design principle by which the geometry of this unique and complex regulatory state pattern is genomically controlled. Each of these boundaries, on either side of the CB, is defined by spatially confined transcriptional repressors, the products of regulatory genes operating across the border of each subdomain. In total, this requires deployment of about ten different repressors, which we identify in this work, thus exemplifying the high informational requirement of spatial regulatory organization during embryogenesis.