The launch of the Al-Rayyan Venue, 24 kilometres (15 miles) west of the capital Doha, marks one of the largest sports gatherings anywhere in the world since the start of the pandemic.
In New Zealand, more than 20,000 fans attended the Super Rugby Aotearoa six days after the country declared itself Covid-free. Similar numbers are attending some National Football League games in the US despite surging infections and deaths.
Fans were able to apply for tickets to Friday's event if they either tested positive for virus antibodies, or tested negative for Covid-19 at accredited clinics in the days before the opening.
Organisers said 10,000 seats would be reserved for each category.
The 40,000-seat ground, which will host seven matches during Qatar 2022 up to and including the round of 16 stage, hosted the domestic Emir Cup final as its inaugural match.
Favourites Al-Sadd, coached by former Barcelona and Spain player Xavi Hernandez, took on minnows Al-Arabi in front of an audience that included the country's ruler, Emir Sheikh Tamim bin Hamad Al-Thani and FIFA boss Gianni Infantino.
Despite strict rules inside the stadium mandating masks, assigning seats, and banning on eating, social distancing was absent in the fan zone before kick-off.
Thousands of spectators, some un-masked, flocked around a stage to watch breakdancing and Bollywood renditions while a compere unsuccessfully encouraged social distancing.
"In theory, no one should have it (COVID-19)," said one organiser as he headed into the stadium ahead of the game.
Security officers confiscated food and drink as well as hand sanitisers under existing rules banning fans from bringing liquids into matches.
"It is very important for everybody. This is the biggest match since March," said Al-Arabi fan Mohammed Mirza, a 60-year-old car dealer from Iran who tested negative for the virus.
"I'm very happy that all the people are safe. For a long time they couldn't come out and see a nice game."
Qatar has slowly been welcoming fans back to stadiums, permitting attendances of up to 30 percent in the top-flight Qatar Stars League.
Qatar, which has tested 43 percent of its 2.75 million population, has recorded 141,716 infections since the beginning of the pandemic with the high rate attributed to aggressive testing and unsanitary accommodation for workers.
However only 242 people have died of the virus and the rate of new infections per 100,000 for the past week was 37.7 -- well down from the peak.