Pima cotton (Gossypium barbadense L.) is grown for its superior fiber quality in four U.S. states and in several other countries. However, there is a lack of information on major and stable quantitative trait loci (QTL) for fiber quality and agronomic traits and abiotic stress tolerance across different environments. In this study, a genetic linkage map based on 403 simple sequence repeat (SSR) markers was developed for the Pima S‐6/89590 intraspecific mapping population consisting of 161 recombinant inbred lines (RILs). Through the evaluation of the RIL population in seven field tests for agronomic traits and fiber quality in the four pima cotton‐growing U.S. states and four greenhouse tests for drought and salinity tolerance, a total of 156 QTL were detected. Eight QTL clusters and four hotspots were further identified, and many of the QTL and their clusters and hotspots were consistent with previous studies that will be useful for marker‐assisted selection. Using a basic local alignment search tool (BLAST) search against the sequenced Pima 3‐79 genome, 26, 16, 32, 14, 127, and 14 candidate genes were predicted for 15 stable QTL on six chromosomes (chromosomes 3, 10, 12, 19, 21, and 24, respectively), for fiber quality traits and abiotic stress tolerance. These genomic regions were rich in genes related to fiber developments and abiotic stress responses. This study provides important information on new and stable QTL across environments for developing superior American pima cotton.