Capsaspora owczarzaki, a protistan symbiont of the pulmonate snail Biomphalaria glabrata, is the centre of much interest in evolutionary biology due to its close relationship to Metazoa. The whole genome sequence of this protist has revealed new insights into the ancestral genome composition of Metazoa, in particular with regard to gene families involved in the evolution of multicellularity. The draft genome revealed the presence of 23 families of transposable element, made up from DNA transposon as well as long terminal repeat (LTR) and non-LTR retrotransposon families. The phylogenetic analyses presented here show that all of the transposable elements identified in the C. owczarzaki genome have orthologous families in Metazoa, indicating that the ancestral metazoan also had a rich diversity of elements. Molecular evolutionary analyses also show that the majority of families has recently been active within the Capsaspora genome. One family now appears to be inactive and a further five families show no evidence of current transposition. Most individual element copies are evolutionarily young; however, a small proportion of inserts appear to have persisted for longer in the genome. The families present in the genome show contrasting population histories and appear to be in different stages of their life cycles. Transcriptome data have been analyzed from multiple stages in the C. owczarzaki life cycle. Expression levels vary greatly both between families and between different stages of the life cycle, suggesting an unexpectedly complex level of transposable element regulation in a single celled organism.