More than 13,000 spectators will be able to attend each day of the Emilia Romagna Grand Prix this year.
The race will take place over the weekend of 31 October and 1 November at Italy's Imola circuit, which last held a Formula 1 race in 2006.
A statement from Imola said it had been "possible to obtain a significant public presence" owing to a "meticulous anti-Covid health security protocol".
Tickets have been on sale for just over a week and some areas are sold out.
Imola is a historic F1 venue that held a Grand for 27 consecutive years from 1980, first as a one-off stand-in for Monza as host of the Italian Grand Prix and subsequently as the San Marino Grand Prix.
It is most famous as the track at which Roland Ratzenberger and Ayrton Senna were killed in high-speed accidents on consecutive days in 1994.
The circuit has been returned to the F1 schedule as the result of the largely Euro-centric calendar constructed by the sport as a response to the coronavirus pandemic.
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F1 has introduced a compressed two-day on-track schedule at Imola as an experiment as it looks to build longer championship seasons moving through the 2020s.
Spectators were kept away from the first eight races of this season, but the Tuscan Grand Prix at Mugello allowed in 2,800 fans a day over its three-day weekend on 11-13 September.
The Russian Grand Prix last weekend also allowed spectators to attend, and the forthcoming Eifel Grand Prix at Germany's Nurburgring on 9-11 October and the Portuguese Grand Prix at Portimao on 23-25 October will also allow limited numbers of fans.
Britain, meanwhile, has called off plans to allow fans back into football matches, with the government saying the earliest they could return is March next year.