In his final days as a schoolboy in 1996, O'Donoghue rang Aidan O'Brien to ask to be his apprentice. O'Brien agreed. The association continued for two decades. O'Donoghue rode his first winner, My Lorraine, at Sligo in 1997. Less than a week later he partnered Theano to a surprise win in the valuable John Roarty Memorial Scurry Handicap at the Curragh on Derby Day, one of the most competitive handicaps of the season. Other trainers began to use him on a regular basis and in October 1999, he partnered Zelden to success in the Derrinstown Stud Apprentice Handicap final at the Curragh. Since then he has won numerous listed, group and other major races in Ireland including the Phoenix Stakes, Noblesse Stakes, Greenlands Stakes, Round Tower Stakes, Debutante Stakes, Ulster Derby, the Irish Cesarewich and the McDonagh Handicap at the Galway Festival. In 2011, O'Donoghue rode the Aidan O'Brien trained Treasure Beach in The Derby, finishing second by a head. Mick Kinane described O'Donoghue's performance on the horse as the best ride in the race. He then won the Irish Derby at the Curragh Racecourse on the same horse. This was his second European classic success following victory in the Poule d'Essai des Poulains, which he won on Astronomer Royal in 2007. Two months later, in August 2011, he won the Shergar Cup at Ascot as a member of the victorious Irish Jockeys' team, winning the 12 furlong Shergar Cup Classic race on Parlour Games, his first ride for Godolphin. In November he was nominated for an Outstanding Achievement Award by Horse Racing Ireland. In January 2012, he was invited to represent Ireland in the Meydan Masters International jockeys challenge in Dubai and in March won the UAE Derby on Daddy Long Legs at the Dubai Carnival meeting. O'Donoghue has ridden for many leading trainers and owners including Aidan O'Brien, Jessica Harrington, Jim Bolger, Dermot Weld and John Oxx in Ireland, Bobby Frankel, Neil Drysdale, Bob Baffert and Todd Pletcher in the US, Lee Freedman in Australia, Dr MAM Ramaswamy, Subaiah Ganapathy and Vijay Mallya in India and Katsuhiko Sumii in Japan. He also won the inaugural running of the American St. Leger at the Arlington Million meeting at Arlington Park in Arlington Heights, Illinois, in August 2012. O'Donoghue won the race on Jakkalberry for the Newmarket based trainer, Marco Botti. From 2016, he replaced Fran Berry as first jockey on the flat for dual-purpose trainer Jessica Harrington, initially mixing that role with his Ballydoyle position. He rode his first Royal Ascot winner, Sword fighter, for Aidan O'Brien in the Queen's Vase in 2016. In 2018, he rode the Harrington-trained Alpha Centauri to win four Group One races, including one at Royal Ascot. O'Donoghue also established a relationship with Godolphin, riding for trainer Charlie Appleby at all eight Dubai World Cup Carnival meetings in 2019. In February 2019, it was announced that Shane Foley would replace O'Donoghue as the Harrington stable jockey. By the following month, it had been announced that O'Donoghue would be used by the new training partnership of John Oxx and Patrick Prendergast.
Major wins
Irish 1,000 Guineas – – Alpha Centauri
Irish Derby – – Treasure Beach
Irish Oaks – – Bracelet
Phoenix Stakes – – Spartacus
---- Great Britain
Coronation Stakes – – Alpha Centauri
Epsom Oaks – – Qualify
Falmouth Stakes – – Alpha Centauri
Yorkshire Oaks – – Seventh Heaven
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Secretariat Stakes – – Treasure Beach
Queen Elizabeth II Challenge Cup Stakes – – Together