Gametic isolation is thought to play an important role in the evolution of reproductive isolation in broadcast-spawning marine invertebrates. However, it’s unclear whether gametic isolation commonly develops early in the speciation process or only accumulates after other reproductive barriers are already in place. It is also unknown whether gametic isolation is an effective barrier to introgression following speciation. Here, we used whole-genome sequencing data and multiple complementary phylogenomic approaches to test whether the well-documented gametic incompatibilities among the strongylocentrotid sea urchins have limited introgression. We quantified phylogenetic discordance, inferred reticulate phylogenetic networks, and applied the Δ statistic using gene tree topologies reconstructed from multiple sequence alignments of protein-coding single-copy orthologs. In addition, we conducted ABBA-BABA tests on genome-wide single nucleotide variants and reconstructed a phylogeny of mitochondrial genomes. Our results revealed strong mito-nuclear discordance and considerable nonrandom gene tree discordance that cannot be explained by incomplete lineage sorting alone. Eight of the nine species examined demonstrated a history of introgression with at least one other species or ancestral lineage, indicating that introgression was common during the diversification of the strongylocentrotid urchins. There was strong support for introgression between four extant species pairs (Strongylocentrotus pallidus ↔ S. droebachiensis, S. intermedius ↔ S. pallidus, S. purpuratus ↔ S. fragilis, and Mesocentrotus franciscanus ↔ Pseudocentrotus depressus) and additional evidence for introgression on internal branches of the phylogeny. Our results suggest that the existing gametic incompatibilities among the strongylocentrotid urchin species have not been a complete barrier to hybridization and introgression following speciation. Their 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.