A significant fraction of living sea urchin species have completely or partially eliminated the pluteus larval stage and instead develop directly from embryo to adult. Direct developing sea urchins develop from large buoyant eggs. We present data to show that evolution of these large eggs is accompanied by the evolution of spermatozoa with elogate heads, in contrast with the conical sperm heads typical of most echinoids. Two congeneric Australian species, Heliocidaris tuberculata, which develops via a pluteus, and H. erythogramma, a direct developer, were investigated in detail. The sperm of H. erythrogramma have an elongate head (11 μm in length) as compared to the conical sperm head (5.6 μm) of H. tuberculata. Electrophoretic analysis of the sperm histones indicates that no unusual histones or protamines are associated with modified head morphology. Genome sizes were determined by flow cytometry. H. erythrogramma has a haploid genome size of 1.3 pg as compared to a haploid genome size of 0.95 pg for H. tuberculata. Other direct developing echinoids have elongate sperm heads, and co-evolution of gametes is indicated as a common feature of evolution of direct development in echinoids. The most extreme case, the direct developing cidaroid sea urchin, Phyllacanthus parvispinus, possesses the longest and narrowest sperm head (20 μm × 1 μm) ever observed in an echinoid.