We describe for the first time reproductive behaviors in the Pirate Perch (Aphredoderus sayanus), a secretive nocturnal fish whose urogenital opening is positioned far anteriorally, under its throat. Some naturalists had speculated that this peculiar morphological condition might serve to promote egg transfer to the fish's branchial chamber for gill-brooding; others hypothesized that Pirate Perch spawn in the substrate of streams but offered no adaptive rationale for the odd placement of the fish's urogenital pore. Here we solve the conundrum through a combination of intensive field investigations, underwater filming, and molecular parentage analyses. We show that Pirate Perch spawn in underwater root masses, the first documentation of such nesting behavior in any species of North American fish. Female Pirate Perch thrust their heads and release their eggs into sheltered canals of these masses. Males congregate at these sites and likewise enter the narrow canals headfirst, to release sperm. Thus, the forward-shifted urogenital pore may facilitate spawning under this special nesting circumstance. We found no evidence of extended parental care. Fish formed their own canals or used burrows made by aquatic macro-invertebrates and salamanders. Genetic analyses based on three polymorphic microsatellite loci demonstrate that a total of at least five to 11 sires and dams were the parents of embryos within each of three assayed root-mass nests (of a total of 23 nests found). Males defended the oviposition sites by body-plugging canal entrances after spawning. This and more direct aggressive behaviors by males probably relate to selection pressures imposed by intense competition for fertilization success under these group-spawning conditions.