Born in Manchester, Borthwick-Jackson joined Manchester United's Academy at the age of 6 in July 2003. He made his debut for the club's reserve team at the age of 16, coming on as a substitute for Tom Lawrence in a 4–1 win over Bolton Wanderers on 16 September 2013. He made 22 appearances for the under-18s during the 2013–14 season, as well as two more in the FA Youth Cup, and got on the scoresheet in the penultimate league game of the season against Stoke City on 29 April 2014.
In July 2014, Borthwick-Jackson played in all five of the under-17s' matches at the Milk Cup, scoring in both the 4–0 semi-final win over Scottish side Partick Thistle and the only goal in the final against French club Vendée. He held a regular spot in the under-18s throughout the 2014–15 season, playing in 28 of their 29 league games, and scoring the second goal in their 2–1 win over Blackburn Rovers on 31 January 2015. However, he also scored an own goal to level the scores against Chelsea on 2 May, before Chelsea went on to win 2–1.
He made the step up to the club's under-21s in 2015–16, and on 7 November 2015, he was named on the first-team substitutes' bench for the first time against West Bromwich Albion; he came on for Marcos Rojo in the 76th minute for his senior debut. Multiple injuries to the squad saw Borthwick-Jackson make his first start on 12 December 2015 away at Bournemouth, ending in a 2–1 defeat. He finished the season with 10 senior league appearances, as well as winning the U21 Premier League.
On 2 May 2016, at the club's annual award ceremony, he won the U21 Player of the Year award after receiving more votes than teammates James Weir and Donald Love. On 30 May 2016, Borthwick-Jackson signed a new contract with United, keeping him at the club until 2020, with the option to extend for a further year.
On 22 August 2016, Borthwick-Jackson joined Championship side Wolverhampton Wanderers on a season-long loan. He made his club debut on 10 September 2016, in a 1–1 draw with Burton Albion. He went on to make a further five league appearances for Wolves up until the appointment of new manager Paul Lambert on 5 November 2016. After which he was phased out of the squad, with his last start being on 5 November 2016 and his last showing on the bench on 10 December 2016. The lack of game time led to Borthwick-Jackson returning to Manchester United to play for the Under-23s in the second half of the season after a mutual agreement between the two clubs was made.
On 7 August 2017, Borthwick-Jackson joined Championship club and rivals Leeds United on a season-long loan for the 2017–18 campaign. His debut came two days later against Port Vale in the EFL Cup, which ended in a 4–1 win. He made his League debut for Leeds on 12 August in a 0–0 draw against Preston North End.
Borthwick-Jackson has represented England at youth level, playing three matches for the under-16s and six for the under-17s. He made his debut for the under-19s against the Netherlands on 12 November 2015.As of match played 22 August 2017
Denzil Haroun Reserve Player of the Year: 2015–16