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Telomeres consist of highly conserved simple tandem telomeric repeat motif (TRM): (TTAGG)n in arthropods, (TTAGGG)n in vertebrates, and (TTTAGGG)n in most plants. TRM can be detected from chromosome-level assembly, which typically requires long-read sequencing data. To take advantage of short-read data, we developed an ultra-fast Telomeric Repeats Identification Pipeline and evaluated its performance on 91 species. With proven accuracy, we applied Telomeric Repeats Identification Pipeline in 129 insect species, using 7 Tbp of short-read sequences. We confirmed (TTAGG)n as the TRM in 19 orders, suggesting it is the ancestral form in insects. Systematic profiling in Hymenopterans revealed a diverse range of TRMs, including the canonical 5-bp TTAGG (bees, ants, and basal sawflies), three independent losses of tandem repeat form TRM (Ichneumonoids, hunting wasps, and gall-forming wasps), and most interestingly, a common 8-bp (TTATTGGG)n in Chalcid wasps with two 9-bp variants in the miniature wasp (TTACTTGGG) and fig wasps (TTATTGGGG). Our results identified extraordinary evolutionary fluidity of Hymenopteran TRMs, and rapid evolution of TRM and repeat abundance at all evolutionary scales, providing novel insights into telomere evolution.