Pharyngeal Arches (PA) are segmental structures, which are bilaterally arranged in the pharynx of all vertebrate embryos. During the segmentation of PAs, the pharyngeal endoderm plays a prominent role to organize each PA by means of reiterative outpocketings called Pharyngeal Pouches (PPs). In gnathostome (jawed vertebrate), the first and second pouches (PP1 and PP2) are concurrently formed earlier than the posterior PPs. On the other hand, the PPs posterior to PP2 are sequentially formed in an anterior to posterior order. Additionally, previous studies in several vertebrate species have clearly shown the mechanisms controlling PP1-2 and PP3-6 development are different. Thus, distinct segmentation systems for the anterior and posterior PPs appear to cooperate in the generation of the complete set of PPs. However, it remains to be elucidated how these distinct systems are coordinated to integrate properly in PP development. Here, we focus on the development of PP2, which develops near the interface point of the two systems. Time-lapse recording and lineage tracing of endodermal cells in transgenic zebrafish showed that the prospective rostral and caudal halves of PP2 are generated in separate locations in the endoderm and then fused together forming PP2. In concordance with morphological observations, the pattern of gene expression throughout PP development supports the idea that there exists two distinct cell populations in PP2. For example, nkx2.3, which is a common PP marker gene, was expressed separately in the rostral and caudal halves before PP2 maturation. We also examined the PP phenotypes of zebrafish mutants for several genes, which were generated using the CRISPR/Cas9 system. Interestingly, we found that in some cases, in PP2, only the rostral- or caudal-half development is impaired. Furthermore, the caudal-half development of PP2 was disrupted by the inhibition of retinoic acid signaling, which is required for the segmentation of PP3-6, in spite of this the rostral half of the PP2 was almost normal. These results suggest that discrete segmentation systems are independently established, and subsequently fused to generate the PP2. This hybrid type of PP organization may have contributed to the evolution of the oropharyngeal system in gnathostomes by segregating the feeding component (mandibular and hyoid arches) from the gill region. Our findings also illustrate the drastic alteration of the developmental mechanisms of the PA, which is the most conserved phylotypic structural characteristic within vertebrates.