Telomeres shorten in replicating somatic cells and with age; in human leukocytes, telomere length (TL) is associated with a host of aging-related diseases. To date, 16 genome-wide association studies (GWAS) have identified twenty-three loci associated with leukocyte TL, but prior studies were primarily in individuals of European and Asian ancestry and relied on laboratory assays including Southern Blot and qPCR to quantify TL. Here, we estimated TL bioinformatically, leveraging whole genome sequencing (WGS) of whole blood from n=75,176 subjects in the Trans-Omics for Precision Medicine (TOPMed) Program. We performed the largest multi-ethnic and only WGS-based genome-wide association analysis of TL to date. We identified 22 associated loci (p-value <5x10-8), including 10 novel loci. Three of the novel loci map to genes involved in telomere maintenance and/or DNA damage repair: TERF2, RFWD3, and SAMHD1. Many of the 99 pathways identified in gene set enrichment analysis for the 22 loci (multiple-testing corrected false discovery rate (FDR) <0.05) pertain to telomere biology, including the top five (FDR<1x10-9). Importantly, several loci, including the recently identified TINF2 and ATM loci, showed strong ancestry-specific associations.