Sulfide mineral framboids associated with fossil bones in marine settings may aid in taphonomic reconstructions because framboids reflect the geochemical conditions under which they form. However, the timing and mechanism(s) of framboid formation on bone remain poorly understood. To better constrain the initial formation of framboids during decomposition of bone in marine depositional environments, we simulated aspects of bone decay on the ocean floor and analyzed framboids found on bone surfaces and in the associated sediment. We observed that framboids formed on bone surfaces within one week of experimentation, and were associated with reducing conditions within a dark-colored microbial mat overlain by oxic waters. Statistical and discriminant analyses of elemental data show that bone-hosted framboids formed in situ on the bone surfaces. Close associations of framboids with sulfidic microbial biofilms indicate that bone-hosted framboids resulted from conditions generated during the microbial degradation of bone-associated organic matter. Our results suggest that framboids can form on bone surfaces while bones rest on the seafloor prior to burial and perhaps prior to the so-called sulphophilic stage of whale-fall animal colonization. We compared experimentally produced framboids with published sedimentary framboid populations. Bone-hosted framboids resemble smaller and less variably sized sedimentary framboid populations canonically known to form in anoxic water columns, even though the bone-hosted framboids were overlain by oxygenated conditions. We propose that the period available for framboid growth is shorter on bone surfaces than in sediments, because geochemical conditions that favor sulfide mineral precipitation on bone are transient. Shorter growing periods and localized conditions result in smaller framboid sizes that may not reflect ambient conditions in a water column.