Telomeres are nucleoprotein complexes that protect eukaryotic linear chromosome ends. They are composed of the telomeric DNA and proteins associated with telomeric repeats. Transcription of telomeric repeats is a conserved feature revealed in many species, and the mechanisms of the telomere homeostasis are closely related to regulation of the telomeric repeat transcription. The telomeres of Drosophila are maintained in the absence of telomerase by the transpositions of the specialized telomeric retrotransposons. Using the Drosophila model, we study the relationship between the telomeric chromatin state and telomeric repeat expression in the female germline. In this study, we have examined the changes in the telomeric chromatin structure and nuclear telomere positioning induced by massive overexpression of telomeric repeats using RNA/DNA fluorescence in situ hybridization, immunostaining and chromatin immunoprecipitation methods. Heterochromatin protein 1 (HP1) and H3K9me3 are important components of telomeric chromatin in different species; however, the mechanisms underlying their deposition at the telomere are not clear. Disruption of the PIWI-interacting RNA pathway causes overexpression of telomeric repeats, a loss of heterochromatic components, and translocation of telomeres from the periphery to the nuclear interior. However, piRNAs are not required either for assembly of the protective telomere capping complex or for telomere clustering in the germline. We have revealed that piRNAs provide a germline–specific mechanism for HP1, Rhino, a germline-specific HP1 homolog, and H3K9me3 deposition at telomeric retrotransposon arrays, thus ensuring telomere silencing at the transcription level during gametogenesis. It has also been found that telomeric transcript levels are regulated by the factors of co-transcriptional RNA surveillance, such as the deadenylase Ccr4-Not complex and nuclear RNA-binding protein Ars2. Noteworthy, the mechanisms for nuclear metabolism of telomeric transcripts are highly conserved. Indeed, Ars2 suppresses transcription of telomeric repeats both in human cells and in Drosophila. Depletion of the factors of co-transcriptional RNA metabolism results in the accumulation of Drosophila telomeric transcripts at transcription sites without the loss of heterochromatin marks. In this case, telomeres remain localized to the nuclear periphery. Taken together, these data indicate that transcription and chromatin states of telomeres rather than accumulation of chromatin-associated telomeric transcripts determine a peripheral localization of telomeres in the Drosophila germline. Funding: Russian Foundation for Basic Research (19-04-00254)