Parc y Scarlets will host Wales' Autumn Nations Cup match against England on 28 November as part of four home games in Llanelli.
It had already been confirmed the Six Nations game against Scotland on 31 October and opening Autumn Nations Cup game against Georgia on 21 November would be held in Llanelli.
Now the England game and a play-off match seven days later will also be held at Parc y Scarlets.
Games will be behind closed doors.
That situation would only change if Welsh Government coronavirus restrictions are changed.
No games this autumn can be played at Principality Stadium in Cardiff as this venue has been in use as the Dragons Heart Hospital.
The WRU had been exploring whether matches could be held in London in front of crowds but current restrictions prohibit that.
Wales are due to host England and Ireland in the 2021 Six Nations in February and March, and will hope the tournament is not held behind closed doors. The Six Nations are also exploring the possibility of the tournament being delayed.
WRU chief executive Steve Phillips said there could be a £35m income loss if all autumn and 2021 Six Nations matches are played behind closed doors.
"It is no secret more than three-quarters of the annual income which supports Welsh rugby at all levels comes directly from our international game and specifically from hosting Wales matches in front of capacity crowds," said Phillips.
"That is why we made contingency plans to play matches in London and why we have waited as long as possible before resigning ourselves to the prospect of playing 'behind closed doors' in Wales.
"This news, however inevitable it may have become during recent days, is a financial set back, but it has not been unforeseen and measures have been and will be taken to mitigate for our losses.
"We understand there is a bigger picture at play and the health of the nation and its individuals, which include our supporters, players, administrators and the many volunteers in our game throughout the country, must come first.
"We know the nation will be tuning in en masse and will be with us at Parc y Scarlets in spirit if not in person and we look forward to the day when we will all be able to gather together once again in more familiar circumstances at Principality Stadium."
The Wales v Scotland game will be the first international rugby match held at Parc y Scarlets with the last Wales international in Llanelli staged in 1998.
"A huge amount of work has gone in behind the scenes from the staff at the Welsh Rugby Union and here at Parc y Scarlets and we are honoured to be the home for the national side for the entire autumn campaign," said Scarlets chief operating officer Phil Morgan.
"We look forward to welcoming Wayne Pivac and the team here this weekend for what promises to be a hugely entertaining first match against Scotland."
In the Autumn Nations Cup, Pivac's side travel to Ireland on 13 November before the three home games.
Finishing positions in the two pools will determine fixtures in the final round, with Wales due to face France, Fiji, Italy or Scotland on 5 December.