It stars by the chilly shores of Lake Michigan and heads southwest through eight states, three time zones and almost 4023km of middle America until it deposits weary motorists beneath the palm trees of California's sun-drenched Pacific coastline.
For 83 years, Route 66 has meandered freely across the national psyche, hymned by Nat King Cole, Chuck Berry and the Rolling Stones as the place to "get your kicks", dubbed "The Mother Road" by Steinbeck, and memorialised by decades worth of Hollywood films, TV shows and documentaries.
Known as the Main Street of America, on account of the myriad communities that prospered along it, and still marked, in some sections, by a shield-shaped logo which appears on T-shirts, coffee mugs, and almost 60,000 items of memorabilia, it is perhaps the most famous road in the history of tarmac.
Yet, amazingly, for a path so well-trodden, Route 66 has until very recently lacked an important - some might say essential - feature: a finish line.
For millions of sightseers, who have set out to travel its entire length, controversy has for years raged over where their journey should formally end.
Some argued the real terminus is on 7th street in Downtown Los Angeles, amid skyscrapers, half an hour inland.
That was where the route officially stopped when it was first created, by an act of Congress, on November 11, 1926.
Others claimed travellers should continue to the location to which it was extended during the 1930s: the junction of Olympic and Lincoln Boulevards in Santa Monica.
But today, that's a soulless, smoggy intersection with nowhere to park.
But most people have chosen to complete their journeys at Santa Monica's 100-year-old pier, which provides a photogenic finish to what amounts to an all-American odyssey.
This week On Wednesday, the pier was finally given what passes for official recognition: amid pomp, circumstance, and a procession of 66 vintage cars, a new sign was unveiled which formally identifies it as the End of the Trail.
The sign is expected to provide a much-needed economic boost to the pier's many stall holders and restaurateurs, including Dan Rice, who owns a nearby kiosk selling a variety of Route 66 souvenirs.
"This gives us the freedom to finally name something officially that everyone else has been doing all along anyway," he said.
The unveiling was not without controversy.
Critics said the new sign effectively re-writes history and described it as a tacky attempt to cash-in on the desire of road-trippers to round off with a memorable photo-shoot.
But that, said its creators, is exactly the point.
"We're not trying to change the past. We're looking to the future and giving people a place where at the end of their journey they can come and fly a kite," said Jim Conkle, the chairman of the Route 66 Alliance, the organisation behind the project.
"You can talk about historic facts all you like. But Route 66 isn't about facts. It's always been about people's memories. It was built on myth. I call it a road that goes through nine states. Eight of them are physical, geographic states. The other one is what you might call a state of mind."
He has a point. It has often been said, over the years, that there are two versions of Route 66.
The first is the road itself: a long stretch of tarmac, large portions of which pass through unremarkable scenery.
The second is the route that exists in the popular imagination: a nostalgic symbol of hope and freedom that brought generations of migrants west to California, 20th century America's version of the Promised Land.
The route was founded in 1926, as one of the first wave of roads to help connect major cities using the newly popular motor car.
While most routes went north to south, or east to west, it passed diagonally from Chicago to Los Angeles, meandering through hundreds of towns and cities which grew prosperous on its motels, restaurants and gas stations.
During the 1920s and 1930s, Route 66 was the road along which hundreds of thousands of "Okies" and "Arkies" from the dust-bowl states of Oklahoma and Arkansas headed west to escape the poverty of the Great Depression.
Many ended up building lives in the farms of California's San Joaquin Valley.
By 1938, it was the first all-tarmac road in America, and the only major route that could take you from the northeast to the west in the depths of winter.
When World War II came along, it provided a crucial supply route to the Pacific, and the Mojave Desert, where General Patton trained his army.
The late 1940s and 1950s, meanwhile, saw it bring tens of thousands more migrants to California to work in the burgeoning aeroplane industry.
By the 1960s it had also become a popular holiday route, carrying families to the Grand Canyon and the newly opened Disneyland.
Over the decades, Route 66 naturally became a cultural institution, not only through The Grapes of Wrath - first a bestselling novel and later a film - but also thanks to countless documentaries and books, together with a TV sitcom called Route 66, which ran for 116 episodes in the 1950s.
It was name-checked in scores of hit songs and inspired many others. Its most recent appearance on the silver screen came in the Pixar film Cars.
Although the road's popularity among motorists declined in the 1980s, with the growing dominance of the interstate highway system (it was formally decommissioned in 1985, bankrupting many businesses) large stretches are still marked with "Historic Route 66" signs and driving along what remains of the road is still a popular tourist activity.
"It's an old road that just refused to die," said Mr Conkle.
"Now, after all these years, it finally has a proper finish. A place to stop, take a photo and make a memory.
"And when it comes down to it, memories are what this old road's always been about."
ON THE ROAD
Opened in 1926, nostalgic Americans call Route 66 "Main Street USA", because it connected eight states: Illinois, Missouri, Kansas, Oklahoma, Texas, New Mexico, Arizona and California.
US Highway 66 - which John Steinbeck called "the Mother Road" in his classic The Grapes of Wrath - featured in scores of Hollywood movies.
After World War II, millions of newly prosperous Americans used it in search of the bright lights of Las Vegas.
By 1970, nearly all of Route 66 was replaced by a four-lane interstate highway.
Bobby Troup's Route 66 is an American classic. The lyrics say: "Travel my way, the highway that's the best. Get your kicks on Route 66."