"It was his first electric guitar and it's what he played at their very early gigs, on their demos and even on their first single, a cover of Chuck Berry's Come On," Charles Epting, director of consignments, pop culture and historical at Heritage Auctions, said.
"This is not a high-end instrument. This is what... somebody working class in the early sixties would have been able to afford, so it's a very humble, modest instrument that paved the way for one of the greatest bands of all time."
Many of the sale items stem from the group's early years, Epting said.
Other items belonging to Jones, who left the group in 1969 and died soon after, include a fringed suede jacket he wore for his final live performance with the band as well as a childhood book.
Also for sale are jackets worn by lead singer Jagger and guitarist Keith Richards as well as drummer Charlie Watts' signed drumsticks.
"The high estimate on the sale is just north of $1.3 million. Obviously, certain key pieces like (Jones') guitar, the jackets we hope will find new homes and could potentially push that price even higher," Epting said.
"I think collector interest will be high from all parts of the world because there are few bands that transcend language, borders, anything like the Rolling Stones."
Highlights of the sale are on show at Heritage Auctions' London office until November 28.
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