Having ridden approximately 300 winners over jumps, Crowley returned to flat racing when he was 27, riding for his sister-in-law, Amanda PerrettatPulborough. In 2010 he became stable jockey for Ralph Beckett.[3] His first Group win came in October 2006 when he rode Hawridge Prince to victory for Rod Millman in the Group 3 Jockey Club CupatNewmarket.[4] His first Group 1 was with the Karl Burke-trained Lord Shanakill in the 2009 Prix Jean PratatChantilly in France.[4] Crowley won the British Champion Jockeys title in 2016, beating the 2015 champion, Silvestre de Sousa, into second place and breaking the record for most winners ridden in a month with 46 victories in September.[3] In November 2016 Jim Crowley was announced as the new number one jockey to leading owner Hamdan al-Maktoum's Shadwell racing operation.[5] His retainer brought him more Group 1 victories and increased prize money at the expense of chasing winners for a second champion jockey title. Shadwell Group 1 winners included the sprinter Battaash, Hukum and Baaeed.[4] Crowley's winning ride on Hukum in the Group 1 King George VI and Queen Elizabeth StakesatAscot in July 2023 proved controversial as the jockey was banned for 20 days and fined £10,000 under the new whip rules for having used his whip nine times during the race, three times over the six allowed.[6]