Aside from polyploidy, transposable elements are the major drivers of genome size increases in plants. Thus, understanding the diversity and evolutionary dynamics of transposable elements in sunflower (Helianthus annuus L.), especially given its large nuclear genome size (ca. 3500 Mbp) and the well-documented cases of amplification of certain transposons within the genus, is of considerable importance for understanding the evolutionary history of this emerging model species. By analyzing approximately 25% of the common sunflower genome from random sequence reads and assembled BAC clones, we show that it is composed of over 81% transposable elements, 77% of which are LTR retrotransposons. Moreover, the LTR retrotransposon fraction is disproportionately composed of chromodomain-containing Ty3/gypsy LTR retrotransposons (‘chromoviruses’), and over 85% of the intact chromoviruses contain tandem chromodomain duplications. We show that there is a bias in the efficacy of illegitimate recombination and homologous recombination in removing LTR retrotransposon DNA, thereby providing insight into the mechanisms regulating transposable element composition in the sunflower genome. In addition, we show that the vast majority of observed LTR retrotransposon insertions have likely occurred since the origin of this species, providing further evidence that biased LTR retrotransposon activity has played a major role in shaping the chromatin and DNA landscape of the sunflower genome.