The progressive bone marrow failure syndrome dyskeratosis congenita (DC) is often caused by mutations in telomerase or the factors involved in telomerase biogenesis and trafficking. However, a subset of DC patients is heterozygous for mutations in the shelterin component TIN2. To determine how the TIN2-DC mutations affect telomere function, we generated mice with the equivalent of the TIN2 K280E DC allele (TIN2^DC) by gene targeting. Whereas homozygous TIN2^DC/DC mice were not viable, first-generation TIN2^+/DC mice were healthy and fertile. In the second and third generations, the TIN2^+/DC mice developed mild pancytopenia, consistent with hematopoietic dysfunction in DC, as well as diminished fecundity. Bone marrow telomeres of TIN2^+/DC mice shortened over the generations, and immortalized TIN2^+/DC mouse embryonic fibroblasts (MEFs) showed telomere shortening with proliferation. Unexpectedly, telomere shortening was accelerated in TIN2^+/DC mTR^−/− mice and MEFs compared with TIN2^+/+ mTR^−/− controls, establishing that the TIN2^DC telomere maintenance defect was not solely due to diminished telomerase action. The TIN2^DC allele induced mild ATR kinase signaling at telomeres and a fragile telomere phenotype, suggestive of telomere replication problems. These data suggest that this TIN2-DC mutation could induce telomeric dysfunction phenotypes in telomerase-negative somatic cells and tissues that further exacerbate the telomere maintenance problems in telomerase-positive stem cell compartments.