Gametic isolation is thought to play an important role in the evolution of reproductive isolation in broadcast-spawning marine invertebrates. However, it remains uncertain whether gametic isolation typically develops early in the speciation process or accumulates after other reproductive barriers are already in place. It is also unknown whether gametic incompatibilities have effectively prevented introgression during later stages of divergence. Here, we use phylogenomic approaches to test whether the well-documented asymmetric gametic incompatibilities between strongylocentrotid urchins have been effective in preventing introgression. Despite a well-supported species tree, we found considerable phylogenetic discordance that cannot be explained by incomplete lineage sorting alone. There was strong support for introgression between at least four pairs of extant taxa: S. pallidus ↔ S. droebachiensis, S. intermedius ↔ S. pallidus, S. purpuratus ↔ S. fragilis, and M. franciscanus ↔ P. depressus. There was additional evidence for introgression on internal branches of the phylogeny. Although gametic incompatibilities may be important in species recognition and the maintenance of species boundaries in strongylocentrotid urchins, gametic isolation does not appear to have been an effective barrier to introgression. The continued divergence in the face of widespread introgression indicates that other reproductive isolating barriers likely exist and may have been more critical in establishing reproductive isolation early in speciation.