Covering 6,842 square feet, the new office space, designed by Brecon-based office interior specialists Bbi, is located at the entrance to the stadium off Westgate Street.
Roger Lewis, Group Chief Executive of the WRU, said: "We have wanted to consolidate our departments for a long time and now our goal of creating a modern environment bringing all our expertise under one roof has been achieved.
"We are very proud of our roots and wanted to retain our presence in the heart of Cardiff. On top of that, Millennium Stadium is our wholly owned subsidiary, it makes commercial sense for us to be based at our home ground and this move will allow a more efficient use of resources.
"This move comes at an important time for us as we enter a new era in Welsh rugby with the appointment of new Coach, Warren Gatland. The prominence of our offices at the entrance of the stadium allows us to welcome the world to Wales and our stadium."
Signifying a change in the office culture of the WRU, the new offices are open plan creating an environment of accessibility and transparency.
To reflect and reinforce the WRU brand, Bbi has specifically chosen interiors influenced by Wales and Welsh rugby for the new headquarters including furniture featuring accent colours of red, white and green, carpet details imitating rugby player formations and rugby ball shaped work tops. For employees having a bad day, Bbi has even installed post protectors for stress relief.
Stephen Price, Account Manager at Bbi, said: "In this project we were able to showcase our work and our abilities. The brief allowed us not only to work on an iconic Welsh building but to be creative in designing a space that reflected the WRU's brand values. Where possible we used environmentally friendly products sourced within Wales so that the offices are both exemplar and sustainable."
Formed in 1989, Welsh headquartered Bbi operates from three locations - Brecon, Leeds and Gloucester - working for some of the UK's leading organisations including Zurich Financial Services and Lloyds TSB Asset Management.
Stephen continued: "As we work on projects across the UK, it is great to be back on home territory for this prestigious scheme."
Mr Lewis added: "We are delighted with the end results. Bbi has managed to take our vision and make it a reality."