Hydrothermal venting, an important cooling mechanism of the Earth, supports a diverse array of seafloor and sub-seafloor ecosystems that are sustained by large thermal and chemical fluxes. Vents have been found along even the slowest and coldest spreading centers, calling into question the driving heat source for these vents. The ultraslow-spreading Mid-Cayman Spreading Center in the Caribbean Sea, which hosts the axial-flank Von Damm Vent Field (VDVF), provides an opportunity to probe the mechanisms for venting at ultraslow spreading rates. Using active-source seismic data from the 2015 CaySeis (Cayman Seismic) experiment, we determined the seismic velocities in the large massif beneath the VDVF. We propose that this massif was produced by a pulse of on-axis magmatism at ca.2 Ma, which was then followed by exhumation, cooling, and fracturing. A low seismic velocity anomaly 5 km below the VDVF is evidence for either a cracking front mining lithospheric heat or intrusive magmatic sills, both of which could drive ongoing deep hydrothermal fluid circulation. We conclude that the transient magmatism and variable crustal thickness at ultraslow-spreading centers create conditions for long-lived hydrothermal venting that may be widespread, and other VDVF-like vents may be common in these areas.