Renowned auction house RM Sotheby's reckons this is the first time a prize of this type has been offered for public sale and estimates the FIA award will fetch between £25,000 and £35,000.
Hill's trophy, rewarding his season-long triumph over Jim Clark while driving for the Bourne-based BRM team, marks the first time a British driver won the F1 crown while driving a British car.
It leads an array of listings from the private Hill family memorabilia collection, with the winner's trophy from the 1972 edition of the 24 Hours of Le Mans also available from £20,000 to £30,000.
PLUS: Graham Hill's 10 greatest races
Then 43, Hill - who won the Monaco GP five times and the Indianapolis 500 in 1966 - became the first driver to earn the so-called 'Triple Crown' of motorsport when he triumphed aboard the Matra MS670 he shared with Henri Pescarolo on what would be his final appearance in the famous enduro.
Earlier this month, RM Sotheby's raised in excess of £2 million for 1992 F1 world champion Nigel Mansell as it auctioned over 320 items from his private collection.
At its Las Vegas sale next month to coincide with the return of a GP to the Nevada city, RM Sotheby's is selling the 2013 Mercedes W04 in which Lewis Hamilton won the Hungarian GP. It is forecasted to go under the hammer for up to £12m.
Among the other Hill-linked items that RM Sotheby's will look to auction in its London sale on 4 November is the cheque for $12,500 that Hill banked for winning the Indy 500. Almost six decades later, the paper it is written on is not expected to reach more than £400.
The first-placed trophy for winning the 1968 Mexican GP, a race which earned Hill his second title and a third constructors' crown for Lotus as he led the team after the death of Clark earlier that year, is predicted to fetch closer to £25,000.
The 1969 Monaco GP winner's pot could make double that, as it marked the final of Hill's 14 top-flight world championship victories.
A period bell helmet decorated in the famous dark blue and white Hill colours carries an estimate of £30,000 while a set of period overalls is valued at £12,000.
Among the more curious items is a 'Freedom of City of London' certificate (£350) and Hill's copy of the 'This is Your Life' book that he was gifted in 1971 (£2000).
A letter from Lord Mountbatten written to Hill's wife Bette following the driver's death in 1975, which says he was recommended for a knighthood, is estimated to sell for up to £550.
