Vastly understudied, mesophotic coral ecosystems lie below shallow reefs (> 30 m depth) and comprise ecologically distinct communities. Brooding reproductive modes appear to predominate among mesophotic-specialist species and may limit genetic connectivity among populations. Using reduced representation genomic sequencing, we assessed spatial population genetic structure (at 50 m depth) in an ecologically important mesophotic-specialist species, Agaricia grahamae among locations in the Southern Caribbean. We also tested for hybridisation with the closely related (but depth-generalist) species Agaricia lamarcki, within their sympatric depth zone (50 m). In contrast to our predictions, no spatial genetic structure was detected between the reefs of Curaçao and Bonaire (~ 40 km apart) within A. grahamae. However, cryptic taxa were discovered within both nominal species, with those in A. lamarcki (incompletely) partitioned by depth and those in A. grahamae occurring sympatrically (at the same depth). Hybrid analyses and demographic modelling identified contemporary and historical gene flow among cryptic taxa, both within and between A. grahamae and A. lamarcki. These results (1) indicate that spatial genetic connectivity in these ecologically important mesophotic species may be maintained over large geographic distances and (2) highlight that gene flow links taxa within this relativity diverse Caribbean genus.