Transposable elements (TEs) are a major component of plant genomes. It is of particular interest to explore the potential activation of TE proliferation, especially in hybrids and polyploids, which often are associated with rapid genomic and epigenetic restructuring. Here we explore the consequences of genomic merger and doubling on copia and gypsy-like Gorge3 long terminal repeat (LTR) retrotransposons as well as on non-LTR long interspersed nuclear elements (LINEs) in allotetraploid cotton, Gossypium hirsutum. Using phylogenetic and quantitative methods, we describe the composition and genomic origin of TEs in polyploid Gossypium. In addition, we present information on ancient and recent transposition activities of the three TE types and demonstrate the absence of an impressive proliferation of TEs following polyploidization in Gossypium. Further, we provide evidence for present-day transcription of LINEs, a relatively minor component of Gossypium genomes, whereas the more abundant LTR retrotransposons display limited expression and only under stressed conditions.