Orthoceratoid cephalopods had straight or slightly curved shells that often contained enigmatic calcareous structures in their chambers. These cameral deposits have been interpreted as counterweights, allowing these cephalopods to assume postures other than a default, downward-facing orientation. These animals must have balanced the proportions of their soft body, cameral deposits, and air-filled chambers to maintain a condition near neutral buoyancy. Lower body chamber ratios (BCRs) allow more mass to be dedicated to cameral deposits, increasing their influence over the total mass distribution. Using 43 computer reconstructions, we calculated the proportion of chamber contents that satisfy a neutrally buoyant condition across different BCRs. Furthermore, we explored the limits of cameral deposit distributions inside the shell to better understand their influence over orientation, stability, and maneuverability. Cephalopods with 40% BCR cannot accommodate any deposits and assume stable, downward-facing orientations. Cephalopods with 30% BCR allow some cameral deposits, which negligibly reduce stability. A slight reduction in BCR to 25% can considerably improve maneuverability, allowing these cephalopods to assume a wider range of postures while swimming. While our results are most relevant to some subset of orthocone cephalopods (Pseudorthoceratida), we also highlight similar constraints faced by broader orthocone groups. Swimming capabilities are extremely sensitive to BCR, which likely constrains the life habits and ecology of these animals. Our results add context to (1) the physical constraints of orthocone cephalopods, (2) their functional complexity in Paleozoic ecosystems, and (3) how these early swimmers navigated physical trade-offs between stability and maneuverability.