Lingard played three times for England at under-17 level in the 2008 Nordic Tournament. He received his first call-up for the under-21 team for the friendly match against Scotland under-21s on 13 August 2013, and made his debut as a second-half substitute for Nathan Redmond as England won 6–0. On 21 June 2015, Lingard came off the bench to score the winner in a 2015 UEFA European Under-21 Championship group match against Sweden.

Lingard was first included in a senior matchday squad on 30 November 2011, in the League Cup quarter-finals against Crystal Palace at Old Trafford, remaining unused as Sir Alex Ferguson’s team lost 2–1 after extra time. He had his only other call-up of the season on 4 January 2012, again unused in a 3–0 away Premier League loss to Newcastle United.

On 6 November 2012, Lingard and teammate Michael Keane joined Leicester City on loan for a month. He made his competitive debut later that day, in a 0–0 Championship draw away to Bolton Wanderers, coming on as a substitute for Martyn Waghorn in the 85th minute. His loan was later extended to 2 January 2013, and he totalled five appearances for the Foxes.

On 27 February 2014, Lingard joined another Championship club, Brighton & Hove Albion, on a 93-day loan. He scored his first goal for the club on 8 April, in a 4–1 win against former club Leicester City, who had sealed promotion to the Premier League days earlier. While with Albion, Lingard played 17 times, including in the Championship play-offs, and scored 4 goals.

On 4 August 2014, Lingard came off the bench to score the third goal in United’s 3–1 International Champions Cup Final win over Liverpool. He made his competitive debut for the club in the first match of the 2014–15 Premier League season at home to Swansea City, starting the match but was replaced by Adnan Januzaj because of injury after 24 minutes. Swansea won 2–1 in Louis van Gaal’s first competitive match as United manager.

On 2 February 2015, Lingard joined Championship club Derby County on loan until the end of the season. He made his first start on 14 February, against Reading in the FA Cup.

On 7 November 2015, Lingard scored his first senior goal for Manchester United in a 2–0 win against West Bromwich Albion at Old Trafford, opening the scoring with a shot past Boaz Myhill from outside the penalty area. On 12 January 2016, he scored against Newcastle United in a 3–3 draw at St James’ Park, with a finish that went between the legs of the goalkeeper after a reverse assist from Wayne Rooney. He added his third goal of the season on 2 February against Stoke City in a 3–0 victory with a closer range diving header from a cross by Cameron Borthwick-Jackson. On 7 February 2016, Lingard scored his fourth goal of the season in a 1–1 draw against Chelsea at Stamford Bridge, breaking the deadlock with a spin and shot inside the penalty area. On 21 May 2016, Lingard scored the winning goal for Manchester United in the 2016 FA Cup Final against Crystal Palace, having come on as a second-half substitute for other goalscorer Juan Mata.

After Michael Carrick and Jamie Vardy withdrew through injury, Lingard received his first call-up to the full England squad, for a friendly against France on 16 November 2015. He did not appear in the match.

Lingard received his next call-up for World Cup qualifiers against Malta and Slovenia in October 2016. He made his debut against Malta, starting on the left wing as England won 2–0. Lingard scored his first goal on 23 March 2018, in a 1–0 win over the Netherlands in a friendly.

Lingard scored the opening goal as Manchester United beat Premier League champions Leicester City 2–1 to win the 2016 FA Community Shield. He scored another important goal in February 2017, this time United’s second of a 3–2 win over Southampton in the 2017 EFL Cup Final. On 6 April 2017, Lingard signed a new contract with Manchester United, of four years with an option for a fifth.

On 5 December 2018, Jesse Lingard scored his first domestic goal of the season in a 2–2 draw against Arsenal. Two weeks later, in the North West derby, Lingard scored his second of the season in a 3–1 loss to Liverpool. During United’s first game under new interim manager Ole Gunnar Solskjær, Lingard doubled his season’s tally, scoring a penalty and a goal from open play in United’s 5–1 win over Cardiff City, in addition to an assist for Anthony Martial. On 25 January 2019, Lingard scored the second goal in a 3–1 win over Arsenal in the fourth round of the FA Cup.

In May 2018, Lingard was named in the 23-man England squad for the 2018 FIFA World Cup. On 24 June, Lingard scored his first ever World Cup goal in a 6–1 victory over Panama during their second group stage match. During the tournament, Lingard received five starts, plus a substitute appearance in the third place play off against Belgium which saw England finish fourth in the tournament.

During the November international break, Lingard scored the first goal in Wayne Rooney’s farewell match against the USA on 15 November. On the following Sunday, Lingard scored the equaliser in 2–1 win over Croatia which put England top of their group and qualified them for the UEFA Nations League semi-finals to be held in June 2019.

He was left out of the England squad for Euro 2020 qualifying matches in October 2019.

On 26 July 2020, Lingard scored his first goal in the final matchday of Premier League; his first since December 2018 in the 98th minute to seal a 2-0 win at Leicester City. His goal secured qualification for the 2020–21 UEFA Champions League and was the final goal of the 2019–20 Premier League campaign.