The repetitive landscapes of mammalian genomes typically display high Class I (retrotransposon) transposable element (TE) content, usually around half of the genome. In contrast, the Class II (DNA transposon) contribution is typically small (<3% in model mammals). Most mammalian genomes also exhibit a precipitous decline in Class II activity beginning roughly 40 million years ago (Ma). The first signs of more recently active mammalian Class II TEs were obtained from the little brown bat, Myotis lucifugus and are reflected by higher genome content (~5%). To aid in determining taxonomic limits and potential impacts of this elevated Class II activity, we performed 454 survey sequencing of a second Myotis species as well as four additional taxa within the family Vespertilionidae and an outgroup species from Phyllostomidae. Graph-based clustering methods were used to reconstruct the major repeat families present in each species and novel elements were identified in several taxa. Retrotransposons remained the dominant group with regard to overall genome mass. Elevated Class II TE composition (3-4%) was observed in all five vesper bats while less than 0.5% of the phyllostomid reads were identified as Class II derived. Differences in satellite DNA and Class I TE content are also described among vespertilionid taxa. These analyses present the first cohesive description of TE evolution across closely related mammals, revealing genome-scale differences in TE content within a single family.