During its life cycle, Trypanosoma brucei shuttles between a mammalian host and the tsetse fly vector. In the mammalian host, immune evasion of T. brucei bloodstream form (BSF) cells relies on antigenic variation, which includes monoallelic expression and periodic switching of variant surface glycoprotein (VSG) gene expression. The active VSG is transcribed from one only of 15 subtelomeric expression sites (ESs). During differentiation from BSF to the insect-resident procyclic form (PCF), the active ES is transcriptionally silenced. In contrast to other eukaryotes, very few telomere-associated proteins have been characterised in T. brucei. We used quantitative interactomics to determine the composition of telomere-associated protein complexes in T. brucei BSF and PCF cells to learn more about the structure and functions of telomeres in trypanosomes. We purified several proteins previously unknown to be telomere-associated, as well as characterised components of telomeres such as TbTRF, TbRAP1, and TbTIF2. Our data suggest different telomere complex compositions in BSF and PCF stages of the parasite. One of the novel telomere-associated proteins, TelAP1, forms a complex with the telomeric proteins TbTRF, TbRAP1 and TbTIF2 and influences ES silencing kinetics during developmental differentiation.