Genetic tools can have a key role in informing conservation management of declining populations. Genetic diversity is an important determinant of population fitness and resilience, and can require careful management to ensure sufficient variation is present. In addition, population genetics data reveal patterns of connectivity and gene flow between locations, enabling mangers to predict recovery and resilience, identify areas of local adaptation, and generate restoration plans. Here, we demonstrate a conservation genetics approach to inform restoration and management of the loggerhead sponge (Spheciospongia vesparium) in the Florida Keys, USA. This species is a dominant, habitat-forming component of marine ecosystems in the Caribbean region, but in Florida has suffered numerous mass mortality events. We developed microsatellite markers and used them to genotype sponges from 14 locations in Florida and a site each in The Bahamas, Belize and Barbuda. We found that genetic diversity levels were similar across all sites, but inbreeding and bottleneck signatures were present in Florida. Populations are highly structured at the regional scale, whilst within Florida connectivity is present in a weak isolation by distance pattern, coupled with chaotic genetic patchiness. Evidence of a weak barrier to gene flow was found in Florida among sites situated on opposite sides of the islands in the Middle Keys. Loggerhead sponge populations in Florida are vulnerable in the face of mass mortalities due to low connectivity with other areas in the region, as well as distance-limited and unpredictable local connectivity patterns. However, our discovery of Florida’s high genetic diversity increases hope for resilience to future perturbations. These results provide valuable insight for sponge restoration practice in Florida.