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“Cuttlebone,” the internalized shell found in all members of the cephalopod family Sepiidae, is a sophisticated buoyancy device combining high porosity with considerable strength. Using a complementary suite of characterization tools, we identified significant structural, chemical, and mechanical variations across the different structural units of the cuttlebone: the dorsal shield consists of two stiff and hard layers with prismatic mineral organization which encapsulate a more ductile and compliant layer with a lamellar structure, enriched with organic matter. A similar organization is found in the chambers, which are separated by septa, and supported by meandering plates (“pillars”). Like the dorsal shield, septa contain two layers with lamellar and prismatic organization, respectively, which differ significantly in their mechanical properties: layers with prismatic organization are a factor of three stiffer and up to a factor of ten harder than those with lamellar organization. The combination of stiff and hard, and compliant and ductile components may serve to reduce the risk of catastrophic failure, and reflect the role of organic matter for the growth process of the cuttlebone. Mechanically “weaker” units may function as sacrificial structures, ensuring a stepwise failure of the individual chambers in cases of overloading, allowing the animals to retain near-neutral buoyancy even with partially damaged cuttlebones. Our findings have implications for our understanding of the structure-property-function relationship of cuttlebone, and may help to identify novel bioinspired design strategies for light-weight yet high-strength foams.