The original members in 1958–59 were:
- From Third Division North: Accrington Stanley, Bradford City, Bury, Chesterfield, Halifax Town, Hull City, Mansfield Town, Rochdale, Stockport County, Tranmere Rovers, Wrexham
- From Third Division South: Bournemouth, Brentford, Colchester United, Newport County, Norwich City, Plymouth Argyle, Queens Park Rangers, Reading, Southampton, Southend United, Swindon Town
- Relegated from Second Division: Doncaster Rovers, Notts County
Of these, Bournemouth, Bradford, Brentford, Hull, Norwich, Notts, QPR, Reading, Southampton, and Swindon have made the top flight in either the First Division or the Premier League era. Stockport, Doncaster, Notts County and Rochdale were the first to be relegated into the Fourth Division the following season (1959–60), starting the bottom-four-team turnover tradition for the third tier. As with the Second Division, the champion and runner-up were automatically promoted; the third place was also promoted automatically beginning in 1974. Play-offs for the third promotion place were introduced in 1987. AFC Bournemouth, formerly Bournemouth & Boscombe Athletic, hold the record as the club to have spent most time in this division.
The Third Division of English football lasted for a total of 72 years, the first 38 years as two regionalised divisions (although just 31 seasons were played due to the advent of World War II) before a 34-year run as a national division. Plymouth Argyle were the most successful team at this level during these years, winning the national title twice, having already won the southern section twice.
In 1992 the FA Premier League started and the Football League was reduced in numbers, leading to the Third Division becoming the fourth tier. See Football League One for subsequent third-tier history.