Digestive system functionality is a key process linked to larval recruitment and survival. However, little is known about organ development and enzyme maturation of the digestive system of North Sea Atlantic herring (Clupea harengus). In this study, herring larvae were reared at 13 °C from hatching to 69 day post hatch, covering four developmental stages: (1) yolk sac (8–9 mm), (2) pre-flexion (9–14 mm), (3) flexion (12–18 mm) and (4) post-flexion stages (15–30 mm). Combined histological (semi-quantitative scoring) and enzyme analyses (pancreatic and intestinal) showed that developmental stages are strongly linked to physiological changes. The larvae lack a functional stomach and use the intestine as the primary site of digestion which is mainly supported by pancreatic enzyme activity. The intestine acquired adult enzymatic digestive features with a functional brush border at the end of the flexion stage and pyloric ceca started to develop during the post-flexion stage. The transition from pre-flexion to flexion stage and the end of the post-flexion stage are energetically taxing periods as indicated by a reduced number and size of liver vacuoles. Based on these findings, we consider these moments as critical periods, where herring larvae could be dramatically affected by suboptimal feeding conditions in the field. This implies that pre-flexion stage larvae with low or no liver reserves may not be able to proceed to the next developmental stage. Hence, the level of energy storage in first-feeding larvae needs to be examined for its use as a field indicator of survival and development.