During liver development, the formation of the bile ducts, hepatic arteries and periportal mesenchyme is interdependent. However, how bile duct development is coordinated with morphogenesis of the vasculature and mesenchyme, and how bile duct lumina form and connect with the canaliculi remains unclear. By combining molecular biology, transgene technology and computational modelling, we found that Slit-Robo signalling, which is active in the mesenchyme, is required for hepatic artery morphogenesis. Furthermore, we propose that the orientation of cholangiocyte division, the dynamics of cholangiocyte differentiation, and osmotic effects are the main drivers of biliary lumen formation. Finally, we provide a first description of how bile duct lumina connect with canaliculi in embryonic livers, and identified Claudin7 as a marker of the cells delineating these junctions.