Lewontin’s paradox, the observation that levels of genetic diversity (π) do not scale linearly with census population size (N_c) variation, is an evolutionary conundrum. The most extreme mismatches between π and N_c are found for highly abundant marine invertebrates. Yet, the influences of new mutations on π relative to extrinsic processes such as N_c fluctuations are unknown. Here, we provide the first germline mutation rate (μ) estimate for a marine invertebrate in corallivorous crown-of-thorns sea stars (Acanthaster cf. solaris). We use high-coverage whole-genome sequencing of 14 parent-offspring trios alongside empirical estimates of N_c in Australia’s Great Barrier Reef to jointly examine the determinants of π in populations undergoing extreme N_c fluctuations. The A. cf. solaris mean μ was 9.13 x 10⁻⁰⁹ mutations per-site per-generation (95% CI: 6.51 x 10⁻⁰⁹ to 1.18 x 10⁻⁰⁸), exceeding estimates for other invertebrates and showing greater concordance with vertebrate mutation rates. Lower-than-expected N_e (~70,000–180,000) and low N_e/N_c values (0.0047–0.048) indicated weak influences of population outbreaks on long-term π. Our findings are consistent with elevated μ evolving in response to reduced N_e and generation time length, with important implications for explaining high mutational loads and the determinants of genetic diversity in marine invertebrate taxa.