Paterson joined the WRU in 1989 and she has served Welsh rugby in a number of areas across the business in the three decades since.
Her roles have seen her dealing directly with strategic and operational matters relating to international, professional, regional and community club rugby.
Paterson was appointed to the Executive Board of the WRU in 2005. In her last role she was the Chair of the Rugby Management Board in Wales and a member of the Professional Rugby Board.
She also represents Wales on the World Rugby Council and Regulatory Committee, European Rugby Board and Guinness PRO14, where she Chairs the Rugby & Regulatory Committees.
She is also on the Board of Great Britain 7s Olympics.
Paterson has been appointed as Director of Rugby at the Six Nations.
She will oversee the collective strategy of the Six Nations in regards to global rugby matters in addition to the rugby strategic direction and rugby operational matters for the championships at all levels.
The senior appointment in addition to the recent CFO, CMO and CCO appointments will further bolster the leadership capabilities and lead Six Nations into a new phase of growth and development.
Paterson said: “It has been an honour to work in Welsh rugby. I am immensely proud of my time at the union but am hugely excited by the challenges and opportunity presented by this new role.
“The Six Nations is unique and I very much look forward to playing my part in ensuring that as a collective we continue to move rugby forward and go from strength to strength.”
WRU chief executive Steve Phillips said: “We wish Julie all the best in her new role with the Six Nations. Her 31-year stint at the WRU was impressive and accomplished.
“Whilst we are sorry to see her leave, it is great that she is staying in the rugby family.
“I have no doubt that she will be as successful in this new position as she was at the WRU and she has my full personal support and that of everyone at the union.”
Ben Morel, CEO Six Nations Rugby commented: “I am thrilled to announce Julie has agreed to join the Six Nations Team.
“Her knowledge of rugby is vast, and her expertise will be a fantastic asset for our organisation.
“She will be a valued addition to our existing leadership team, and I am looking forward to working with her on the development of our sport.”