Now 58, the man who was one of the guiding lights both on and off the field in the transformation of Pontypool from the also-rans of Welsh rugby into the most feared and successful side in the UK, and who won two Grand Slams and three Triple Crowns during a 19 cap Test career with Wales, is stepping down for 'personal reasons'.
He will officially leave the Union at the end of July. No successor is likely in the short term while the WRU general manager Steve Lewis conducts his strategic review of the Union's Directorate.
'I've spent the best part of 40 years working in rugby as a player, coach, selector and administrator and I feel the time is right for me to step down,' said Cobner.
'I'm fiercely proud of Welsh rugby and I'm proud of the contribution I have made to the game that has given me so much in my life. But now is the time for me to put my family first.
'I've thoroughly enjoyed the eight years I've spent heading up the Directorate at the WRU and I feel we have made massive strides since 1996.
'Welsh rugby now has a very capable, nationwide network of development officers who are working to enhance and nurture our national game from grass roots level upwards and I firmly believe we are moving in the right direction.
'Let's face it, the game has seen tumultuous change over the past 10 years and is unrecognisable from when I was playing. If we haven't always managed that change well, the signs are there for all to see that we now have strong, professional leadership in Wales and a structure that merely needs time and fine-tuning to bring the best out of our resources.'
The work of the Directorate is currently being overseen conjointly by WRU general manager Steve Lewis and Cobner's assistant, Mostyn Richards.
Cobner announced his decision to the WRU chairman, David Pickering, last week.
'The contribution made by Terry Cobner to Welsh rugby has been immense. It is up there with the all-time greats in the Union's 123 year history,' said Pickering.
'His achievements at Pontypool are legendary, his work with and in the Wales and Lions packs in the seventies was world renowned and he went on to become an influential national coach and selector.
'When he left Wales to work at Oundle School many felt he had been lost to our game. But he was enticed back in 1996 as our first Director of Rugby and his list of achievements over the past eight, turbulent years means he leaves us with an invaluable legacy.
'In his time at the Union he has revolutionised our coach education structure, built a clear and much envied Player Development Pathway, rationalised the boundaries of age group rugby, formulated an Academy Structure for regional and national levels and given clear guidance on regional rugby.
'There is no doubt that Terry's retirement will leave us with a huge gap to fill at the WRU, but everyone who knows him and his family will fully understand the reasons behind his decision.
'While we wish Terry, his wife Brenda and their children all the best for the future, the game in Wales must say a huge and heartfelt 'Thank You' to Terry for his great work on behalf of Welsh rugby.'