The WRU says one of its teams will be based in the capital Cardiff, one in the west and one in the east.
It means one of the two regions in the west, Llanelli-based Scarlets or Swansea-based Ospreys, will be defunct, while Cardiff and the Dragons offered the respective capital and east licences.
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The WRU Board says the licensing framework and the licence award process will begin in December 2026 and conclude by the end of the 2026/27 season at the latest.
Professional Rugby Board chair Marianne Okland said: "There is now a duty on all of us involved in the professional game in Wales to work together to determine a shared future operating model. How we progress over the forthcoming months will be critical."
