Ayling began his career at Arsenal joining the club at the age of 10. He was part of Arsenal youth team's double-winning team of the 2008–09 season, before signing his first professional contract in July 2009. Ayling was loaned out to Yeovil Town in March 2010 and played four matches. At the end of the season he agreed a permanent deal with Yeovil. After four seasons with Yeovil, Ayling signed for Bristol City.
Ayling was born in Lambeth, London. He joined Arsenal at the age of 10, despite being a Chelsea fan, progressing through the Arsenal youth teams, playing alongside Jack Wilshere, before signing scholarship forms with the club in the summer of 2007. Ayling featured in the Reserves whilst he was still a schoolboy, and was an integral part of Arsenal youth team's Premier Academy League and FA Youth Cup double-winning team of the 2008–09 season, forming a crucial defensive partnership with Kyle Bartley. In June 2009, Ayling signed his first professional contract with Arsenal.
Ayling's only call into the first-team squad came during the 2009–10 season. Ayling was an unused substitute for a dead rubber 1–0 UEFA Champions League group stage defeat to Greek team Olympiacos on 9 December 2009. Ayling departed the club in June 2010 after his contract expired.
In March 2010, Ayling joined League One club Yeovil Town on loan for an initial month, and on 2 April 2010, made his professional debut as a second-half substitute in a 0–0 draw away at Southend United. Ayling's loan was extended until the end of the season, Ayling played four matches in total, including his first league start in the final match of the season against Brighton & Hove Albion, on 8 May 2010.
On 30 June 2010, Ayling agreed a permanent contract with Yeovil. He made his debut in a 2–1 victory over Leyton Orient. Ayling made forty appearances in his first full season with Yeovil but had discipline issues receiving thirteen yellow and two red cards. On 19 May 2013, Ayling played in the 2013 League One play-off Final at Wembley Stadium as Yeovil beat Brentford 2–1 to earn promotion to the Championship.
After relegation from the Championship during the 2013/14 season with Yeovil Town, his contract expired at the end of the season in June 2014. After rejecting the offer of a new contract at Yeovil, he left the club.
Following his departure from Yeovil Town, Ayling signed for their fellow League One club Bristol City on 8 July 2014 for an undisclosed compensation fee, signing a three-year deal. Ayling made his debut for Bristol City, on 9 August 2014, in their opening day victory over Sheffield United.
During the 2014–15 season, Ayling won the Football League Trophy, with Bristol beating Walsall 2–0 at Wembley Stadium on 22 March 2015. On 18 April 2015, Ayling impressed for Bristol City playing 58 matches that season in all competitions as they were crowned League One champions following a 0–0 draw at home to Coventry City and earned promotion to the Championship. Playing 33 times either playing right back or centre back during the 2015/16 season in the Championship, Ayling's form at the back helped Bristol City retain their Championship status.
On 11 August 2016, Ayling signed for Championship club Leeds United for an undisclosed fee on a three-year contract. Ayling made his debut for Leeds in a 2-1 loss to Birmingham City on 13 August 2016. With first choice right back Gaetano Berardi out injured, Ayling started the season as the clubs first choice right back, his impressive form also kept Berardi out the team despite Berardi's return from injury in October. On 7 November, Ayling was named in the English Football League Team of the Week after his impressive performance in Leeds' 3–2 victory against Norwich City.
On 9 August 2017, he captained Leeds for the first time when he was named as captain for Leeds' League Cup tie 4–1 win against Port Vale.
Former Guardian sports writer Steve Claridge lauded Ayling for his "reading of the game, communications skills, organisation skills, aerial prowess, two footedness and use of the ball" in his scouting reports column.As of match played 12 September 2017
ArsenalPremier Academy League: 2008–09
FA Youth Cup: 2008–09
Yeovil TownFootball League One play-offs: 2012–13
Bristol CityFootball League One: 2014–15
Football League Trophy: 2014–15