We have recently shown that telomeres in cells that utilize the recombination-mediated alternative lengthening of telomeres (ALT) pathway elicit a DNA damage response that is partly independent of telomere length. We therefore investigated whether ALT telomeres contain structural abnormalities, and whether these contribute to ALT activity. Next generation sequencing was used to analyze the sequence content of telomeres in cells that employ either ALT or telomerase. We found that variant repeats are interspersed throughout the telomeres of ALT cells, presumably as a consequence of recombination-mediated copying events involving the variant repeat-rich proximal regions of telomeres, and subsequent spread throughout the telomeres. The TCAGGG variant repeat predominates and creates a high-affinity binding site for the nuclear receptors TR4 and COUP-TF2, which have previously been found to bind to ALT telomeres. In addition, we demonstrate that nuclear receptors are directly recruited to telomeres following incorporation of TCAGGG repeats using a mutant telomerase. Variant repeat incorporation induces ALT-associated characteristics but not inter-telomeric recombination. We propose that the presence of variant repeats throughout ALT telomeres and the consequent binding of nuclear receptors alter telomere architecture and contribute to the recombination permissive state.