The first match in the new £5.7m ground situated in the shadow of BT Murrayfield will take place on Saturday, September 11 with a curtain-raiser against Newcastle Falcons.
The Scottish Building Society Pre-season Series will also see Edinburgh take on Benetton Rugby at their new home a week later on Saturday, September 18. Both matches kick-off at 3pm.
The games will mark the start of the Mike Blair era after the former Edinburgh and Scotland captain took over as the Pro14 club's new head coach following the departure of Richard Cockerill last month.
Edinburgh will have a number of new faces in the line-up for the forthcoming campaign including Argentina internationals Emiliano Boffelli and Ramiro Moyano, Blair's first signings following his appointment.
The matches will also see the return of fans, with the new purpose-built arena able to hold up to 7800 supporters, around 5,800 seated and 2000 safe-standing, under covered stands on all four sides.
The matches are included in Edinburgh’s season-ticket offer for the 2021-22 campaign.
Tickets go on general sale on Thursday morning at 10am starting at £5 for U18 and £10 for adults, with the club expecting high demand for a place in the stands for these opening games.
Douglas Struth, Edinburgh Rugby managing director, said: “We’re delighted to receive the continued backing of Scottish Building Society who sponsor the first-ever Edinburgh Rugby matches to be played in our new purpose-built home.
“It’s a significant moment in Edinburgh Rugby history and, with back-to-back Saturday afternoon kick-offs, we’re hoping to create a real festival atmosphere in and around the ground, where we can celebrate the return of rugby together as a club, alongside our supporters, who’ve waited so patiently to finally step foot in their new home.
“We’re really looking forward to hosting two quality opponents in Newcastle Falcons and Benetton Rugby. Both matches will give our supporters a taste of what’s to come in 2021/22, with Head Coach Mike Blair now at the helm and several new signings ready to pull on the blue and orange jersey.
“We continue to work hard behind the scenes on our plans for our first crowd at the ERS and make this and every game a great occasion."
The Edinburgh Rugby Stadium was completed in February and is the team's first permanent home since its inception as a professional side in 1996 and as an amateur district select dating back to 1872.
The completion of the project includes World Rugby certification for contact training and playing on the new state-of-the-art 3G surface, meaning the Edinburgh squad are also able to train in the ground.
Struth added: “All of us - players, staff and management - cannot wait to see our supporters back in stands next season, and that first match against Newcastle Falcons will be a celebratory and in many ways emotional moment as we acknowledge just how far we’ve come as a club through this pandemic."