Trabeculation is a crucial process during heart development which describes the protrusion of cardiomyocytes into the lumen of the ventricular chamber to form complex muscular structures called trabeculae. Defects in this process results in various human disease such as left ventricular non compaction cardiomyopathies and other congenital heart defects. Several cellular mechanism have been identified underlying trabeculation including cardiomyocyte selection, depolarization, delamination, and proliferation. However, the molecular mechanisms governing trabeculation are still poorly understood. Previously, we have shown that gpr126 is required for trabeculation and heart development in mice and zebrafish. Gpr126 is an adhesion G-protein coupled receptor which is autoproteolytically cleaved into an N-terminal fragment (NTF) and a C-terminal fragment (CTF). Here, we show that NTF and CTF control different cellular processes during trabeculation. CTF-depleted mutants gpr126^st49 (expressing NTF) were characterized by a multilayered ventricular wall lacking any trabecular projections. This is in contrast to our previous results obtained with morpholinos suggesting that the NTF is sufficient for proper heart development in zebrafish. A molecular characterization of gpr126^st49 mutants revealed that cardiomyocytes in the multilayer fail to depolarize and relocalize N-cadherin from the lateral to the basal side. This explains why gpr126^st49 mutants fail to form trabeculae and indicates that all cardiomyocytes in the multi-layered wall fail to attain a trabecular identity. In addition, these cardiomyocytes showed significantly upregulated myocardial notch expression, which is known to prevent cardiomyocytes from attaining a trabecular identity. These data suggest that the NTF is required for proper compact wall formation, whereas the CTF is required for proper formation of trabeculae. We analyzed the full length-depleted mutant gpr126^stl47 in regards to compact wall integrity. 20% of gpr126^stl47 maternal zygotic mutants exhibited complete absence of trabeculation and 35% hypotrabeculation. Analysis of these mutants revealed defects in proper cellular localization of N-cadherin. Instead of being specifically localized at the lateral side, N-cadherin was mainly distributed to the apical and basal side in the cardiomyocytes of the compact myocardial layer. This indicates that the NTF is required for the proper localization of N-cadherin during heart development to contribute to the formation of trabeculae. This hypothesis was substantiated by the observation that mosaic myocardial overexpression of NTF resulted in local cardiomyocyte multilayering. Finally, overexpression of gpr126 in the absence of Erbb2 signaling and blood flow /-or contractility failed to cause multilayering suggesting that Gpr126 is part of the well established ERBB2 signaling cascade controlling trabeculation. Collectively, our data support a model with domain-specific functions of gpr126 in trabeculation, where the NTF of Gpr126 is required for priming the compact layer at the onset of trabeculation by maintaining cell-cell junctions, while the CTF helps in providing trabecular identity to cardiomyocytes through modulation of myocardial notch.