The diocese took the college over in 1957 and appointed Patrick Mulligan, a Fermanagh native, as its first president. Classes ran from a building on East Bridge Street in the centre of Enniskillen while a new campus was constructed at Drumclay. In September 1963 the buildings were complete and the move was made. Mulligan oversaw the planning, the build, and the first two extensions, which raised the roll from 200 students to 300. There were boarding facilities for about sixty boys. In 1966, a second expansion added four new classrooms, a modern-languages department, a laboratory, a bookstore, and a teachers' recreation room. The college has continued to expand since. By the late 2010s it had over 700 students, fifty teaching staff, and thirty-five support staff. Mulligan was appointed Bishop of Clogher within three years of leaving the principalship, served until 1979, and died in 1991.

Gaelic football is the soul of St Michael's. The MacRory Cup, the Ulster Colleges' senior football championship, has been lifted by St Michael's seven times, putting the school in the top six in the competition's history. After early wins in 1973 and 1992, the great spell came at the turn of the millennium: finals in four consecutive years, with the cup taken in 1999, 2001, and 2002. Another title came in 2012, beating St Patrick's College in Maghera 0-09 to 1-04. On 18 March 2019, St Michael's took the MacRory home again, beating Omagh CBS 0-16 to 2-06 in Armagh. Three weeks later, on Saturday 6 April 2019, they did something the school had never done before. In the Hogan Cup final at Croke Park, in front of a national audience, St Michael's beat Naas CBS 1-12 to 1-11. By one point. By a single point in injury time. The all-Ireland title was theirs.

Every year the school holds a run around the grounds in memory of Oisin McGrath, a former pupil who died after a playground incident. The money raised supports the Oisin McGrath Foundation, set up in his name. The run draws students past and present and threads through Drumclay for a few hours each year, and is the kind of small, persistent ritual that defines what schools mean to the communities around them. The list of notable former pupils carries the cultural weight of Catholic Fermanagh in the late twentieth century: the artist T. P. Flanagan (1929 to 2011), the independent nationalist MP Frank McManus, the poet and former editor of The Honest Ulsterman Frank Ormsby, the actor Ciaran McMenamin, the broadcaster Fearghal McKinney, the All-Star Gaelic footballer Barry Owens, the writer Nigel McLoughlin, and the Sinn Fein MLA Phil Flanagan.

On 11 June 2025, at Dungannon Crown Court, the former president of St Michael's College, Canon Patrick McEntee, was unanimously convicted on eight counts of historical indecent assault against four children. The offences had occurred between 1978 and 1989. McEntee had joined the school staff as dean in 1977, succeeded Macartan McQuaid as president in 1994, served in that role until 2000, and remained on the school's board of governors until 2021. Judge Richard Greene described him as a 'predatory paedophile' and sentenced him on 12 September 2025 to seven years in prison. He will be on the sex offenders register for the rest of his life. McEntee was not the only abuser on the staff during that period. Father John McCabe, who taught at the school from 1977 until 1988, had been jailed in 1995 on thirteen sex offences. The then Bishop of Clogher, Joseph Duffy, chairman of the school's board of governors, had been aware of McCabe's abuse in 1989 and failed to report it to police, social services, or the school where McCabe subsequently took up employment. In 2025 the current Bishop of Clogher, Lawrence Duffy, on behalf of the board, issued a formal apology to victims. The PSNI urged further survivors to come forward. Former students have since spoken publicly about what they call 'disturbing' experiences during those years. The children who suffered were not curiosities of an unhappy era. They were boys who had been sent to a school by parents who trusted the men running it, and that trust was systematically betrayed.

Cathal O'Connor, a former pupil of St Michael's and a teacher there for twenty-two years, was confirmed as the new principal in March 2025, taking over from Mark Henry. In April 2025 the Council for Catholic Maintained Schools announced that St Michael's and St Joseph's College, Enniskillen, would be amalgamated when St Joseph's closes in early 2027, with declining pupil numbers cited as a key reason. The amalgamated school will not use academic selection. The college now also faces a four-month PSNI investigation into a series of severe bullying incidents reported in September 2025. The school stands at a difficult crossroads: an institution with a real record of athletic and academic achievement, a long list of alumni who shaped Catholic Fermanagh, and an obligation, finally and publicly acknowledged, to face what was done to children inside its walls. The buildings at Drumclay carry both stories. The pupils walking past them now will have to learn both.