Horizontal transfer (HT) is the transmission of genetic material by means other than parent-to-offspring: a phenomenon primarily associated with prokaryotes. However, eukaryotic genomes contain transposable elements (TE), colloquially known as 'jumping genes' for their ability to replicate to new genomic locations. Long interspersed element (LINE) retrotransposons are TEs which move using a "copy and paste" mechanism, resulting in gene disruptions, chromosome rearrangements and numerous diseases such as cancer. LINEs are autonomous; they can move into a new genome and immediately commence replicating. This makes them good candidates for HT. Growing evidence shows that HT is more widespread than previously believed, although questions still remain about the frequency of HT events and their long-term impact. Here we show that LINE-1 (L1) and Bovine-B (BovB), the two most abundant retrotransposon families in mammals, were initially introduced as foreign DNA via ancient HT events. Using a 503-genome dataset, we identify multiple ancient L1 HT events in plants and show that L1s infiltrated the mammalian lineage after the monotreme-therian split, in contrast with the current literature. We also extend the BovB paradigm by identifying: more than twice the number of estimated transfer events compared to previous studies; new potential blood-sucking parasite vectors and occurrences in new lineages (e.g. bats, frog). Given that these retrotransposons make up nearly half of the genome sequence in today's mammals, our results provide the first evidence that HT can have drastic and long-term effects on the new host genomes. This revolutionizes our perception of genome evolution to consider external factors, such as the natural introduction of foreign DNA. With the advancement of genome sequencing technologies and bioinformatics tools, we anticipate our study to be the first of many large-scale phylogenomic analyses exploring the role of HT in genome evolution.