Mr Flowers played for the Black Country club between 1952 and 1967 and helped them to three First Division titles, and the FA Cup in 1960.
Wolves paid tribute to Mr Flowers, tweeting: "We are deeply saddened to announce the passing of club legend and vice president Ron Flowers MBE at the age of 87.
"A giant on the pitch and a gentleman off it.
"There will be many people remembering Ron today and all of our thoughts are with those who knew and loved him."
Mr Flowers played 515 times for Wolves, placing him fifth on their all-time appearances list.
He joined from Wath Wanderers, a Wolves nursery club, and established himself as a key creative player in the side managed by Stan Cullis.
He also played 49 times for England and featured in 40 consecutive international matches between November 1958 and April 1963, which included the 1962 World Cup in Chile.
However, Mr Flowers did not feature as Sir Alf Ramsey’s men became world champions on home soil in 1966, but received a World Cup winner’s medal at Downing Street in 2009 after only those on the field at the final whistle initially got one.
He left Wolves the year after to join Northampton, where he served as player-manager, followed by spells at Telford and Wellington Town.
Mr Flowers was awarded an MBE in the 2021 New Year Honours List.