Transposable elements (TEs), so called “jumping-genes”, are DNA sequences that are able to proliferate in the genomes of organisms. Their movement in the genome can be disruptive by inserting either into or near genes, but sometimes they provide beneficial mutational variation that natural selection, the ultimate force in evolution, can act upon. Despite their potential benefits for the organism, their overall movement is often thought to be at odds with the rest of the genome leading to them having been referred to as selfish. To counteract the negative effects of TE’s movement, hosts have evolved defenses to control and prevent TE-related damage. In this thesis, I have studied TEs in fungi and their interaction with a fungal specific defense called repeat induced point mutation (RIP). RIP induces C-to-T mutations in any repeated region of the genome, including both TEs and duplicate genes. One of the key species where RIP has been described is the filamentous ascomycete Podospora anserina, which has been used as a model organism within genetics and evolution for over a century. In chapter I we were able to dive deeply into the interaction between a specific TE called crapaud and its evolutionary history, and discuss its potential interaction with RIP. In chapter II we discovered that RIP have been lost in a close relative to P. anserina called Podospora pseudocomata and that this loss may have been the cause of a total shift in both types and amount of TEs in its genome. This species also has smaller centromere regions than P. anserina. The centromere regions are the anchoring points when the chromosomes are pulled apart in every cell division. In many fungi the DNA of this region contains many TEs, and our result hints at a connection between the centromeres and RIP. P.anserina and P. pseudocomata are both part of an order known as Sordariales, which have species important to industry and contain model organisms such as P. anserina and Neurospora crassa. In chapter III we compared the genomes of nine families from this order using whole genomes and constructed a phylogeny of the order using phylogenomics. In chapter IV we developed in-depth methods to continue investigating RIP in the order Sordariales and discovered that P. pseudocomata is not the only species that has lost the RIP mutation pattern. We find 17 species lacking RIP, spread across the Sordariales phylogeny. In conclusion, this thesis presents a glimpse into the world of TEs and host genomes and their defense against TEs in filamentous ascomycetes, and the balance and conflict between them.