The spread of mobile genetic elements within and between the genomes of diverse organisms has greatly impacted biology across the tree of life. Inteins are an enigmatic type of mobile genetic element capable of self-splicing at the protein level. While inteins are generally rare in eukaryotes, we have discovered that three strains of the newly described eukaryotic microbe Anaeramoeba have many dozens of inteins encoded in their nuclear genomes. Genomic investigation shows that Anaeramoeba’s inteins were acquired by lateral transfer from viruses and bacteria, and subsequently spread to many different genomic locations via allelic and, possibly, non-allelic homing. The promiscuous nature of inteins in Anaeramoeba makes them promising substrates for genetic engineering and biotechnological applications.