When first discovered, spliceosomal introns presented a paradox for evolutionary biology — why are eukaryotic genomes filled with mostly unnecessary and sometimes costly elements? In recent years, a suite of molecular functions are attributed to introns, but the proximate origins of new introns are largely obscure. By evaluating all sequenced eukaryotic genomes, we showed that specialized transposable elements (TEs), introners, generate thousands of new introns in hundreds of species from across the tree of life. Virtually all known types of TEs create new introns, and direct evidence indicates that introners can arise in new lineages through horizontal gene transfer from distantly related species. Using a combination of experimental evolution and population genomics within species containing active introner families, we show that while most new introns are deleterious or neutral, a noteworthy subset is highly advantageous. Therefore, new introns will accumulate in eukaryotic genomes as a virtually inevitable consequence of ongoing conflicts between TEs and their hosts, and offer opportunities for rapid adaptation.