Offshore facies of the Mesoproterozoic Sulky Formation, Dismal Lakes Group, arctic Canada, preserve microbialites with unusual morphology. These microbialites grew in water depths greater than several tens of meters and correlate with high-relief conical stromatolites of the more proximal September Lake reef complex. The gross morphology of these microbial facies consists of ridge-like vertical supports draped by concave-upward, subhorizontal elements, resulting in tent-shaped cuspate microbialites with substantial primary void space. Morphological and petrographic analyses suggest a model wherein penecontemporaneous upward growth of ridge elements and development of subhorizontal draping elements initially resulted in a buoyantly supported, unlithified microbial form. Lithification began via precipitation within organic elements during microbialite growth. Mineralization either stabilized or facilitated collapse of initially neutrally buoyant microbialite forms. Microbial structures and breccias were then further stabilized by precipitation of marine herringbone cement. During late-stage diagenesis, remaining void space was occluded by ferroan dolomite cement. Cuspate microbialites are most similar to those found in offshore facies of Neoarchean carbonate platforms and to unlithified, buoyantly supported microbial mats in modern ice-covered Antarctic lakes. We suggest that such unusual microbialite morphologies are a product of the interaction between motile and non-motile communities under nutrient-limiting conditions, followed by early lithification, which served to preserve the resultant microbial form. The presence of marine herringbone cement, commonly associated with high dissolved inorganic carbon (DIC), low O2 conditions, also suggests growth in association with reducing environments at or near the seafloor or in conjunction with a geochemical interface. Predominance of coniform stromatolite forms in the Proterozoic—across a variety of depositional environments—may thus reflect a combination of heterogeneous nutrient distribution, potentially driven by variable redox conditions, and an elevated carbonate saturation state, which permits preservation of these unusual microbialite forms.