Born in Islington, London, Carruthers was playing football local to his hometown of Hatfield, Hertfordshire when he was signed by Cambridge United's under-10 side. He trained frequently with Manchester United, but when Cambridge United abandoned their youth team set-up he signed for Arsenal, the team he supported as a child. He went on to represent Arsenal at under-18 level and captained the club's under-16 side. However, in 2009 Carruthers rejected offers from Fulham and Arsenal in favour of a move to Aston Villa.
Carruthers signed for Aston Villa in June 2009, aged 16. He made his name playing for the club's reserve and academy sides as an attacking midfielder and winger. Following a number of injuries to Alex McLeish's first team squad in the latter stages of the 2011–12 season, the young midfielder was brought in to train with the first team on a number of occasions.
Carruthers made his first-team debut in Villa's 1–1 Premier League draw at Liverpool on 7 April 2012, replacing Barry Bannan for the final four minutes. He made two further substitute appearances that month.
On 1 April 2013, Carruthers captained Aston Villa's youth squad to the final of the NextGen Series where they beat Chelsea 2–0, at the Stadio Giuseppe Sinigaglia, in Como, Italy.
Carruthers was sent out on loan to League One side Milton Keynes Dons on 10 August 2013 on a youth loan until 4 January 2014. He made his debut against Preston North End on 17 August. Coming on as a substitute in the 56th minute, Carruthers won a penalty, which was in turn converted by Shaun Williams, levelling the score at 2–2. A week later Carruthers scored within 15 minutes of coming on as a substitute against Bristol City, hitting a left footed effort into the top corner to earn another 2–2 draw. On 8 January 2014 it was announced that he had extended his loan spell at Milton Keynes Dons until April.
On 6 August 2014 it was announced that Carruthers had signed for Milton Keynes Dons on a three-year deal for an undisclosed fee. He scored his first goal of the season on 13 September in a 5–3 away win against Barnsley. On 25 April 2015 he scored a second goal, opening a 3–2 win over Rochdale at Spotland. Eight days later the team earned their first promotion to the Championship with a 5–1 home win over Yeovil Town on the final day, with Carruthers setting up the first goal from Carl Baker.
On 3 January 2017 it was announced that Carruthers had signed for Sheffield United on a three-and-a-half year deal for an undisclosed fee, thought to be worth £250,000.
Carruthers is of Irish, Italian and Moroccan descent and is eligible to play for Italy, Morocco, England and the Republic of Ireland, the country of his grandparents. In 2011, he made his debut for the Republic of Ireland U19 team. On 10 September 2012 Carruthers made his debut for the Republic of Ireland U21 team away to Italy.
On 15 March 2016, whilst attending the Cheltenham Festival at Cheltenham Racecourse, Carruthers and Northampton Town's James Collins were photographed urinating into a beer glass whilst standing on a balcony. The following day, Carruthers apologised for his behaviour, and following a meeting with MK Dons manager Karl Robinson and chairman Pete Winkleman he was fined two weeks' wages and suspended by the club. He pledged his fine to charities, including one chosen by the racecourse.As of match played 30 April 2017