The chitin‐based peritrophic matrix (PM) is a structure critical for both gut immunity and digestion in invertebrates. PM was traditionally considered lost in all vertebrates, but a PM‐like chitinous membrane (CM) has recently been discovered in fishes, which may increase the knowledge on vertebrate gut physiology and structural evolution. Here, we show that in zebrafish, the CM affects ingestion behavior, microbial homeostasis, epithelial renewal, digestion, growth, and longevity. Young mutant fish without CM appear healthy and are able to complete their life cycle normally, but with increasing age they develop gut inflammation, resulting in gut atrophy. Unlike mammals, zebrafish have no visible gel‐forming mucin layers to protect their gut epithelia, but at least in young fish, the CM is not a prerequisite for the antibacterial gut immunity. These findings provide new insights into the role of the CM in fish prosperity and its eventual loss in tetrapods. These findings may also help to improve fish health and conservation, as well as to advance the understanding of vertebrate gut physiology and human intestinal diseases. Synopsis The chitinous membrane (CM) is an essential gut structure in invertebrates that was considered lost in vertebrates, but was recently discovered in fish. This study shows that it has differential roles in zebrafish digestion and gut immunity. The presence of the CM affects ingestive behavior, gut homeostasis, microbiota, digestion, growth, and longevity. The CM is not a prerequisite for fish survival, reproduction, and gut immunity against bacteria. CM absence results in age‐dependent gut inflammation and atrophy. The CM has an important role in fish health, conservation, prosperity, and diversity. The chitinous membrane (CM) is an essential gut structure in invertebrates that was considered lost in vertebrates, but was recently discovered in fish. This study shows that it has differential roles in zebrafish digestion and gut immunity.