Gene therapy has become a widely accepted treatment for inherited or acquired genetic diseases. Lentiviral vectors are of particular interest because of their favorable biosafety profile and ability to introduce their therapeutic cargo into non-dividing cells. For clinical use, these viral vectors must be generated under conditions of good manufacturing practice in large quantities, which currently are provided via transient production. A solution for stable, robust, easy to scale, cost-effective, and predictable production of the therapeutic vectors is currently not available. Here, we describe the design, generation, and characterization of EL1-820, a packaging cell line for the stable production of lentiviral self-inactivating (SIN) vectors pseudotyped with the envelope glycoprotein of vesicular stomatitis virus. EL1-820 enables the introduction of a lentiviral SIN-vector expression cassette via Flp-recombinase-mediated cassette exchange (RMCE) into a predefined locus selected for optimal vector production, with expression units designed to improve reliability. EL1-820-based producer clones generated similar titers (1 × 107 TU/mL) from a targeted, single-copy integration of a lenti-GFP or a lenti-chimeric antigen receptor transfer vector as transient production. In initial scale-up experiments, multiple harvests from bioreactors could be achieved, resulting in titers of around 8-9 × 107 TU/mL after tangential flow filtration and a total yield of about 2.3 × 1011 TU. In conclusion, RMCE-based introduction of the transfer construct allows stable, defined, predictable, and safe vector production suitable for clinical applications.