Telomeres are nucleoprotein complexes with a crucial role of protecting chromosome ends. It consists of simple repeat sequences and dedicated telomere-binding proteins. Because of its vital functions, components of the telomere, for example its sequence, should be under strong evolutionary constraint. But across all plants, telomere sequences display a range of variation and the evolutionary mechanism driving this diversification is largely unknown. Here, we discovered in Monkeyflower (Mimulus) the telomere sequence is even variable between species. We investigated the basis of Mimulus telomere sequence evolution by studying the long noncoding telomerase RNA (TR), which is a core component of the telomere maintenance complex and determines the telomere sequence. We conducted total RNA-based de novo transcriptomics from 16 Mimulus species and analyzed reference genomes from 6 species, and discovered Mimulus species have evolved at least three different telomere sequences: (AAACCCT)n, (AAACCCG)n, and (AAACCG)n. Unexpectedly, we discovered several species with TR duplications and the paralogs had functional consequences that could influence telomere evolution. For instance, M. lewisii had two sequence-divergent TR paralogs and synthesized a telomere with sequence heterogeneity, consisting of AAACCG and AAACCCG repeats. Evolutionary analysis of the M. lewisii TR paralogs indicated it had arisen from a transposition-mediate duplication process. Further analysis of the TR from multiple Mimulus species showed the gene had frequently transposed and inserted into new chromosomal positions during Mimulus evolution. From our results, we propose the TR transposition, duplication, and divergence model to explain the evolutionary sequence turnovers in Mimulus and potentially all plant telomeres.