Verticillium wilt is one of the most devastating soilborne diseases in lettuce and the use of host resistance is the most optimal choice for its management. This study focused on identifying and mapping the genetic loci for resistance against Verticillium dahliae race 3 in a mapping population of 200 F2:3 families developed from a cross between moderately resistant red-leaf lettuce 'Sentry' and susceptible green leaf lettuce 'La Brillante'. The population was genotyped using the tunable Genotyping by Sequencing (tGBS) approach. An ultra-high-density genetic linkage map containing 34,838 single nucleotide polymorphism (SNP) markers grouped into 1,734 bins was constructed using F2 progeny and a sliding window approach. Three quantitative trait loci (QTLs) for resistance to V. dahliae race 3 were located on linkage groups (LGs) LG 2 (qVR3-2.1), and LG 4 (qVR3-4.1 and qVR3-4.2). Each of these QTLs explained up to ~10% of the total phenotypic variation for the trait. At each locus, the resistance alleles were derived from cultivar ‘Sentry’ that is partially resistant to the pathogen. Additional resistance loci to the disease are expected in this population, and transgressive segregation indicates that some of those loci could originate from the susceptible cultivar ‘La Brillante’. Candidate genes linked to some of the QTLs for V. dahliae race 3 resistance, plant development, and leaf color were identified. The QTLs for resistance identified in Sentry may diversify the resistance gene pool and provide an alternative tool to manage a newly emerged V. dahliae race 3.