The British & Irish Lions played in Cardiff against a World XV in 1986 and against Argentina in 2005.
It will also be the Lions' first match in Scotland.
Japan, who reached the World Cup quarter-finals on home soil last year, will not play Test rugby for the entirety of 2020 due to Covid-19 restrictions but Gatland is looking forward to a stern test against Jamie Joseph's side next year.
The Lions, who traditionally tour Australia, New Zealand or South Africa every four years, will be playing Japan for the first time, with the match to be held at Murrayfield on June 26.
"One of our objectives is to give Warren and the playing squad as much meaningful preparation as possible before departing on tour, so we are delighted to have agreed this fixture", said Ben Calveley, the managing director of the British & Irish Lions.
However, despite a series of offers from the Lions, including compensation and also moving the dates of the tour, the Premiership has refused to move its final and reiterated that its players would not be released to take part in the fixture - even if they were not involved in the final - as the match falls outside World Rugby's regulation nine, which governs player release for internationals.
But the Welsh, Irish, Scots and Saracens picked will be able to take to the field days before the Lions fly to South Africa.
"We saw Japan play some excellent rugby during the World Cup and they will come to Edinburgh fully-motivated to win", Lions head coach Warren Gatland said in a statement.
World Cup hosts Japan reached the quarter-finals past year, defeating Ireland, Scotland, Samoa and Russian Federation in pool play before losing to eventual champions South Africa.
"I hope that many rugby fans from around the world will witness the historic match between the Lions and Japan and enjoy the brand of rugby to be showcased by each side".
"It's a chance for the matchday squad to put hands up for Test selection".
"We all know that Lions tours need to have fans in there, without that famous sea of red, Lions tours are just not the same", he said.
"It is truly a once-in-a-lifetime opportunity for our players, and we can't wait for it to come".
The 2021 Premiership final means Gatland is unlikely to have a full squad to choose from for the Japan fixture, with some absentees possibly involved in the English season climax.
Tickets for the Japan game go on pre-sale early next month, but it remains to be seen if the coronavirus pandemic has any impact on it.
"It is a great honour for us to be able to play a Test match against the British & Irish Lions", commented Mori.
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