Flavivirus such as dengue virus (DENV), West Nile Virus (WNV), are a serious threat to public health. The flavivirus single stranded RNA genome is translated into a polyprotein cleaved by viral and cellular proteases into three structural proteins and seven non-structural proteins. Non-structural (NS) protein 3 is a multifunctional protein with N-terminal protease and C-terminal helicase. The NS3 protease requires co-factor NS2B for enzymatic activity and folding. The NS2B-NS3 viral protease cleaves the viral polyprotein. Due to its essential role in viral replication, NS2B-NS3 protease is an attractive target for antiviral drugs. Despite availability of crystal structures, dynamic interactions of the N- and C-termini of NS2B co-factor have been elusive due to their flexible fold. In this study, we employ integrative structural approaches combined with biochemical assays to elucidate the interactions of flexible NS2B/3 N- and C-termini. We identified a novel cis-cleavage site between NS2B/NS3. Mapping of NS2B N- and C-termini with NS3 indicates that these interdomain interactions occur exclusively on the solvent exposed beta-barrel of NS3 protease domain. Our integrative approach enables a comprehensive understanding of the folding and dynamic interactions of DENV NS3 protease and its cofactor NS2B.