The widespread and abundant brooding brittle-star (Amphipholis squamata) is a simultaneous hermaphrodite with a complex mitochondrial phylogeography of multiple divergent overlapping mtDNA lineages and can exhibit high levels of inbreeding or clonality and unusual sperm morphology. We use exon-capture and transcriptome data to show that the nuclear genome comprises multiple (>3) divergent (π > 6%) expressed components spread across the mitochondrial lineages, and encompassing several other genera, including diploid dioecious dimorphic species. We also report a massive sperm genome size in A. squamata, an order of magnitude larger than in the sperm of other brittle-star species, consistent with our genetic measures of elevated and variable ploidy (>6). We propose that A. squamata (and related taxa) is a hybrid polyploid complex with many independent hybrid origins, variable ploidy, and complex patterns of parental subgenomes. We hypothesize that A. squamata has facultative sperm-dependent asexual reproduction, where sperm is required for embryogenesis but the egg and sperm only occasionally undergo fertilisation, a process that has been associated with the formation of polyploid hybrid swarms in other taxa. Unique amongst known marine allopolyploids, the A. squamata complex inhabits an extensive bathymetric as well as geographic range. Measuring site heterozygosity in next-generation sequencing data is an effective way of screening samples for allopolyploidy and reproductive assurance, particularly for under-researched taxa such as marine invertebrates.