Reigning champions Chelsea will kick off their Barclays FA Women's Super League defence at Manchester United.
Emma Hayes' side were declared champions on a points-per-game basis following the termination of the league in May due to the impact of the coronavirus pandemic.
Chelsea will travel to Casey Stoney's United on the opening weekend of the season, with the Football Association confirming the opening two rounds of fixtures for the WSL and Women's Championship 2020-21 season.
Manchester City, who were leading the league when play was halted, head to promoted Aston Villa in what will be Gareth Taylor's first match at the helm.
The Women's Championship also gets under way on the weekend of September 5/6, with relegated Liverpool welcoming Durham.
The full fixture list for both divisions will be released in early September, with the FA confirming that the season is "due to start behind closed doors until it is safe for fans to return".
Kelly Simmons, the FA's director of the women's professional game, said: "Fans have had to wait a while to see some live action and being able to announce the first two rounds of fixtures ahead of so many other leagues was something we really pushed for to build up the excitement ahead of the season starting.
"We're really looking forward to seeing our players back on the field to show off their talent and showcase the very best of what the Barclays FA Women's Super League and FA Women's Championship have to offer.
"My hope is that they will be joined by supporters in our stadiums soon, because fans make the matchday experience even more special.
"Once again fans will be able to stream Barclays FA Women's Super League fixtures on The FA Player that are not chosen for broadcast, while selected FA Women's Championship matches will also be streamed live."