The c-Jun N-terminal kinase (JNK) is part of a mitogen-activated protein kinase (MAPK) signaling cascade that is regulated in part by scaffold proteins. Scaffold proteins simultaneously associate with various components of the MAPK signaling pathway and play a crucial role in signal transmission and regulation. However, the precise mechanism by which scaffold proteins function is still lacking. WDR62 is a novel JNK-binding protein that was isolated in our lab using the Ras recruitment system in yeast. WDR62 has no sequence homology to any known protein. We demonstrate that WDR62 specifically associates with JNK but not with ERK and p38. WDR62 interacts with all JNK isoforms through a conserved D domain motif located at the C-terminus. Furthermore, a synthetic peptide composed of the WDR62 docking domain inhibits JNK2 activity in vitro. WDR62 associates with the JNK2-activating kinase MKK7b1 isoform but fails to interact with MKK7a1. The fact that WDR62 associates with both JNK and MKK7 suggests that WDR62 is a novel JNK scaffold protein. Recently it was found that recessive mutations within WDR62 result in severe brain malformations, such as microcephaly. One such mutation corresponds to a WDR62 protein with truncation in its C-terminus that preserves both JNK and MKK7 docking domains, yet fails to associate with them. We show that this C-terminus that is lacking in the mutant protein is composed of three putative α-helices with the last one forming a dimerization domain. The dimerization is necessary for JNK and MKK7 association. Importantly, fusion of the WDR62 dimerization mutant to a functional heterolougous dimerization motif was able to reconstitute WDR62-JNK association but not the association of MKK7, demonstrating that WDR62 dimerization is critical for its scaffolding function. Furthermore, this novel domain is highly conserved and is shared by MAPKBP1 JNK scaffold protein enabling its homodimerization and heterodimerization with WDR62.