Ammonia is a promising fuel for marine propulsion and generation, yet its acute toxicity and associated safety challenges necessitate careful consideration. Current regulations recognize the hazards of ammonia, introducing numerous technical safety measures in response. However, the effectiveness of these measures in ensuring acceptable risk levels for future vessels remains to be fully assessed. This study estimates the risk level onboard ammonia-powered ships, identifying the aspects with the largest and controllable influence on it. Three hypothetical concepts of ammonia fuel supply were developed in this study on an example tanker vessel and analyzed using the quantitative risk assessment (QRA) methodology. The obtained risk profiles were evaluated against the risks by an equivalent liquefied natural gas-fueled system, serving as a benchmark. The results demonstrate that ammonia-fueled ships exhibit individual risk levels for engineering crew with periodic duties in fuel preparation rooms (FPR), or similar compartments, which are 1–1.5 orders of magnitude higher than those observed for a conventional gas-fueled alternative. An analogous increase has been noted for the public potentially present onboard or in proximity. The study underscores the importance of managing human-machine interactions, enhancing the reliability of supply systems, and managing the systems’ complexity to mitigate risks in FPRs. Regarding public safety, the analysis highlights new risk mechanisms introduced by ammonia and examines how storage conditions affect exposure levels. By offering a detailed QRA framework, this research contributes to the development of effective risk management strategies for ammonia-powered ships.