We had demonstrated that reprogramming-induced epigenome remodeling in human induced pluripotent stem cells (hiPSCs) resulted in the mobilization of endogenous retrotransposons LINE-1 [L1], Alu and SVA, and that intronic L1 de novo insertions occuring during reprogramming and hiPSC cultivation, interfere with host gene expression. Here, we set out to identify those specific loci among the ~1 Mio genomic L1 insertions that encode retrotransposition-competent L1 (RC-L1) elements which are expressed and mobilized in human pluripotent stem cells (hPSCs), causing deleterious insertions. To this end, we generated individualized, custom-tailored genomes of two human embryonic stem cell lines and six hiPSC lines and their parental cells by mapping all fixed and polymorphic RC-L1 loci of these cell lines, and identified 13 fixed and 104 polymorphic RC-L1 loci in these cell lines. To quantify transcripts expressed from the L1-specific promoter of RC-L1 loci, we applied RNA-seq and the 5'RACE method combined with PacBio sequencing, which facilitated mapping of L1-specific RNA reads to unique genomic L1 loci. We mapped those RC-L1 loci that are transcribed in the pluripotent state identifying potential source elements responsible for L1-mediated retrotransposition in hPSCs. Subsets of only 29-63 of the 78-97 cell line-specific polymorphic RC-L1 loci were found activated in hiPSCs relative to their parental cells. One to six specific RC-L1 loci were responsible for ~50 % of all RC-L1 transcripts. Unexpectedly, 75 of 117 RC-L1 loci identified in hPSCs were shown to be mobilized in cancer cells, and of those, 55 were also expressed in hPSCs. In sum, we uncovered small subsets of 22-54 specific RC-L1 loci that are transcribed and mobilized in each analyzed hPSC line including L1 source loci reported to be responsible for deleterious mobilization events observed in various cancer types. Our findings underscore the significant potential of expressed RC-L1 elements as endogenous mutagens in hPSC.