Some tracks among the list of 10, like Sebring, Watkins Glen and Long Beach, were rather successful in their era - but fell away from use as the sport expanded and moved on.
Others like Las Vegas, Detroit, Dallas, Phoenix and Indianapolis had their moments, but ultimately failed to deliver the huge impact in the country that F1 hoped they would.
With Austin's Circuit of the Americas already on the calendar, F1 is trying again to make a further breakthrough in the Land of the Free. Thus, it has embarked upon a 10-year journey to host a second race, the Miami Grand Prix, from 2022.
The decision to hold the race has been heralded by F1 CEO Stefano Domenicali as an important moment for the championship as it bids to build a brighter future.
"We are proud, and this is not me, we are proud as F1 because we are looking ahead,” he said at the announcement of the new race at Imola last weekend.
“We are putting the foundations for an incredible future of F1. And this is a milestone that we all wanted.
"Just last night, when we shared the information with all the teams, everyone was really: 'Wow, that's the right way to go, this is really where we should be'. So this is really the direction we're going to take for a great future for F1."
But despite the optimism, some remain cynical about whether or not the current Miami project will really deliver as much of an impact as the original plan several years ago for a race near the city’s port.
Back then, F1 was going to blast over one of Miami’s main bridges, and have a spectacular backdrop to the race that would have confirmed the venue as one of a ‘destination’ events.
Now, running around a car park (albeit a large one) outside a stadium, there are fears it may not deliver quite the same ‘wow’ factor.
Domenicali himself brushes aside such concerns. He is adamant that the Miami stadium plan does not mean that F1 has fallen short in its ambitions to make Miami a major event.
“It's great, it's not a compromise,” he said. “As always, when you look for a different solution, you need to consider all the elements that make everyone happy.
“There were lots of discussion for a different layout. I'm sure that the track you are going see around the Miami Hard Rock Cafe and Miami Gardens will be fantastic. We have built up something that will be spectacular.”
Race promoter Tom Garfinkel, CEO of the Miami Dolphins, believes the new solution is actually an improvement over the original downtown plan.
For while running a track around a car park may spark bad memories of F1’s Las Vegas event, he thinks it is actually a positive: because it has given the track designers a clean sheet of paper
“I think it's going to be a lot better in certain respects,” he said.
“When we originally looked at the city design, you have a lot of constraints around the racetrack and the first priority was creating a great racing circuit for the drivers for fans, with multiple passing opportunities.
“When we looked at the Hard Rock site, we had basically a blank sheet of paper to work with designers and to work with F1. Obviously the FIA put together a racetrack that is dynamic in a lot of ways, hopefully.
“Plus, to be able to put on great experiences that are uniquely reflective of the diversity of Miami and everything we do, we have existing infrastructure there, and things in place. We think we're in a better position to be able to do that.”
Garfinkel thinks the stadium environment will allow the race promoters a better opportunity to give fans the experience they want: plus guarantee spectacular views of the circuit.
“If you look at what we did with the Miami Open Tennis Tournament, for example, what we're going to be able to do is completely transform [the area] into a campus with landscaping and all kinds of different opportunities and food and beverage areas,” he explained.
“We want to create an environment where people are blown away when they get there. And I think again, starting with a sort of a blank sheet of paper, we’ve been able to design a circuit with the designers and F1 and the FIA that has a lot of passing opportunities.
“There's going to be vistas from the stadium which sits at the centre of the circuit. You could walk around the top deck of the stadium and see every turn in the racetrack. I think that's a pretty unique opportunity.
“It's going to be beautiful and I don't really see any limitations. In fact I just see opportunities.”
The Hard Rock plan ticking the boxes for F1 and fans at the track is just one part of the equation, though, for the key for the sport is in using the grands prix to ensure the whole of the United States finally becomes enthralled by the championship.
F1’s plan to make sure that the country’s two grands prix in Miami and Austin are kept separate on the calendar is a means to try to spread out the spikes of interest, plus ensure each event can maximise its promotion.
And, while Austin has given F1 the most permanent home it has had in the USA for years, F1 is still seeking the next step: something extra special that will grab the interest of the public and general media to help increase the sport’s reach.
The USA audience is still relatively small – around 1 million viewers on TV from an overall population of 328 million.
There is huge untapped potential but, if there ever was an opportunity to capitalise and make inroads, it is now.
One factor that cannot be underestimated in trying to predict F1’s latest push in to the United States is the fact that its profile is much different now to what it was even five years ago.
Where once, a seven time world champion like Michael Schumacher was happily able to go on holiday there without being recognised, now the success of the Netflix: Drive to Survive series has changed everything.
Not only are all the drivers now celebrities, but other big personalities in the paddock – such as McLaren CEO Zak Brown – have become well known.
“I had [television personality] Michael Strahan come up to me in a restaurant and he would not have any clue who I was if it wasn’t for Netflix,” Brown said recently during a trip to the IndyCar season opener.
“He came up to me in a New York restaurant. Super polite guy, loves McLaren, and the first thing he’d say was ‘I’ve seen you on Netflix.’ So I think it’s definitely made a difference around the world, but specifically in America.”
The Netflix effect was cited by computer technology giant Oracle as one of the reasons why major American companies had shown a bigger interest in the sport this year after arriving as major sponsors.
The opportunity for F1 in the USA has never been bigger than now. But it’s one thing talking about making a breakthrough in the market, it’s quite another actually going out there and conquering the country.
The Miami deal has been done, but the hard work has only just started.