The ten founding members in 1964–65 included Home Farm, Bray Wanderers, Athlone Town, Shamrock Rovers B plus the reserve teams of Shelbourne, Bohemians, St Patrick's Athletic, Dundalk, Drumcondra and Drogheda. The 1965–66 season saw the league expanded to include twelve teams. Bray Wanderers dropped out, while Dalkey United, Ormeau and Tullamore Town all joined. Early sponsors of the league included Blackthorn Cider and Castrol. During the early seasons teams competed for two trophies. The Blackthorn Trophy was initially awarded to the overall winners of the league. The Castrol Trophy was awarded to the winners of a single round league. The 1967–68 season saw Belgrove replace Ormeau, Athlone Town win the Castrol Trophy and Shamrock Rovers B win the Blackthorn Trophy. In 1968–69 Athlone Town won both the Castrol Trophy and Blackthorn Trophy, finishing six points clear of St Patrick's Athletic. The following season, 1969–70, saw Athlone Town take up a place in the League of Ireland senior division. In 1970 UCD were elected to the League of Ireland B Division. Their senior team would continue to play in the B Division until 1979–80 when they were elected to join the Senior Division. Among the players who played for UCD during this time were Kevin Moran and Hugo MacNeill. In the 1978–79 McNeill was UCD's top scorer was with 46 goals. A popular myth also alleges that Sócrates may have played for UCD during time. In 1975 Dublin University also joined and they were coached by Liam Tuohy. Hugo MacNeill would also play for Dublin University
Dalkey United controversy
During the mid-1970s Dalkey United enjoyed moderate success while playing in the B Division. In 1973–74 they won the FAI Intermediate Cup and between 1975 and 1976 and 1977–78 they won the Blackthorn Trophy three times in a row. However their time in the league would end in controversial circumstances. Frank Mullen described the B Division as the "most incompetent" league Dalkey United had ever been involved with. Clubs without a senior team in the League of Ireland "were treated very unfairly". It was not uncommon for Dalkey United to travel to away games against Waterford United or Dundalk only to find the game postponed. No compensation for travel expenses would be offered either. In the 1977–78 season Dalkey United were due to travel to Dundalk to play in the quarter-final of the Blackthorn Trophy. However a few days before the game was due to be played the Dundalk manager, Jim McLaughlin, phoned the Dalkey United chairman to request the game be postponed due to heavy snow. Dalkey United agreed and Dundalk subsequently informed the league the match was cancelled. However a few weeks later the semi-final draw was made and Dalkey United found themselves excluded. The club informed the league that the quarter-final against Dundalk had not been played, only to be told that the semi-finals were going ahead regardless. Dundalk were ordered to play the semi-final or face expulsion from the competition. Dalkey United opted to take legal action and the case was heading for the High Court when the league decided to declare semi-final results null and void. After winning the rescheduled quarter-final against Dundalk, Dalkey United then won the semi-final and went on to defeat Bohemians in the final at Dalymount Park. Having won the Blackthorn Trophy for a third time in a row, Dalkey United resigned from the league immediately afterwards and never applied to rejoin. They subsequently joined the Leinster Senior League.
In 1983–84 Athlone Town Reserves won the B Division title, now known as the Egan C&C Trophy. Other teams in the B Division this season included Dublin University, Monaghan United, Longford Town, St Brendan's, Belgrove, Shamrock Rovers B and the reserve teams of Waterford United, Dundalk, Shelbourne, Drogheda, St Patrick's Athletic, Bohemians and UCD. The Athlone Town team included Fran Hitchcock, John Caulfield and Turlough O'Connor, who was their highest goalscorer. O'Connor had earlier played for Town in the same division back in its debut season of 1964–65.
UCD title
In 1997–98, after 28 years of membership, UCD won its first ever B Division title. Their B team finished their 24-match campaign unbeaten.