Welbeck made his England under-16s debut as a 14-year-old in October 2005 against Wales in the Victory Shield, which England won that year. He then progressed to the England under-17s team, scoring the decider in a qualifying match against Serbia, to help his team progress to the 2007 UEFA European Under-17 Championship. The tournament saw England finish as runners-up to Spain, which secured the team a place in the 2007 FIFA U-17 World Cup in South Korea. There, Welbeck scored two goals against New Zealand, helping Scotland to reach the quarter-finals in their first involvement in the tournament. Welbeck was originally intended to be a squad member for England’s European Under-19 Championship campaign in July 2008, but was forced to withdraw. He eventually made his debut for the under-19s on 9 September 2008, playing the full 90 minutes in a 2–1 win over the Netherlands.

Welbeck was first spotted by Manchester United as a six-year-old. At eight years old, he impressed with local team Fletcher Moss, and was finally picked up by the Manchester United youth academy. He joined United during the 2005–06 season, making his debut for the club’s under-18 team on 8 April 2006 in a league match against Sunderland. He then came on as a substitute in the next match, before being named as an unused substitute in the team’s last two matches of the season. The following season, he made a further 28 appearances for the under-18s, scoring nine goals, including eight appearances and one goal in the FA Youth Cup, in which he helped the team to reach the final, despite being two years younger than some of the other players. He was not handicapped despite suffering from Osgood–Schlatter disease, and was making rapid progress, despite his pneumonia.

Welbeck signed his first trainee contract in July 2007, and started the 2007–08 season in the under-18 team, but was quickly promoted to the reserve team, making a number of substitute appearances. Then, in January 2008, he was called up to the first team for the trip to Saudi Arabia to play Al-Hilal in Sami Al-Jaber’s testimonial match. Welbeck made his debut in that match on 21 January 2008, coming on as a 65th-minute substitute for Anderson. Welbeck had the chance to snatch a draw for United when he was brought down in the penalty area in the final minute, but he put the penalty kick over the bar.

He joined the first-team squad partway through the 2007–08 season, and made his competitive debut for the Manchester United first team on 23 September 2008, starting up front in a 3–1 home win against Middlesbrough in the League Cup Third Round. Welbeck’s Premier League debut was made on 15 November 2008, coming on as a 63rd-minute substitute for Park Ji-sung against Stoke City. He marked his debut with a curling 30-yard shot into the top right corner for United’s fourth goal in a 5–0 win. He started in the 2009 League Cup Final at Wembley Stadium on 1 March 2009, in which United beat Tottenham Hotspur 4–1 on penalties after a 0–0 extra-time draw.

On 18 November 2008, it was reported that the Ghana Football Association was keeping tabs on Welbeck, with a view to him representing the Ghana national team in the future. On 29 March 2011, Welbeck was called up to the England squad, for their friendly fixture against Ghana. Welbeck replaced Ashley Young in the 81st minute of a 1–1 draw with Ghana at Wembley Stadium.

On 23 September 2009, Welbeck scored his first goal of the 2009–10 season, the only one of the match in the League Cup Third Round against Wolverhampton Wanderers. Welbeck made his UEFA Champions League debut in a 1–0 home defeat to Beşiktaş in November 2009. The following month he signed a new contract, keeping him at Manchester United until 2013.

Welbeck made his England under-21 debut on 10 February 2009, in the 3–2 loss to Ecuador, coming on for Adam Johnson. He followed this up with another substitute appearance in a 2–0 home defeat to France on 31 March. He was then named in Stuart Pearce’s original 23-man squad for the 2009 UEFA European Under-21 Championship in Sweden on 27 May, but he had to pull out of the squad on 31 May, due to an injury. On 7 September 2010, Welbeck scored his first two goals for the England under-21 team in a 3–0 win over Lithuania. He scored his third under-21 goal in a 4–0 away victory over Denmark on 24 March 2011. Welbeck then started the first match of England’s campaign at the 2011 UEFA European Under-21 Championship against Spain. Welbeck scored an 88th-minute equaliser as England began the tournament with a 1–1 draw.

On 25 January 2010, Welbeck became Alex Ferguson’s son Darren Ferguson’s first signing as Preston North End manager since he took charge earlier in the month, signing on loan for the remainder of the 2009–10 season. As part of his recovery, he took part in a training session at Manchester United’s training ground, but his knee swelled up again. The injury required surgery and Welbeck’s loan was cut short on 16 March so that he could return to Manchester United for the operation.

On 12 August 2010, Welbeck became Steve Bruce’s eighth summer signing after Sunderland signed the United striker on loan for the duration of the 2010–11 season. His debut for Sunderland came on 14 August as an 83rd-minute substitute for Darren Bent in a 2–2 home draw against Birmingham City. On 14 November, Welbeck scored his first Sunderland goal as he completed the scoring in a 3–0 away victory over Chelsea, rounding off what was described as an “impressive individual performance”. Eight days later, Welbeck scored his first home goals for Sunderland, striking twice in a 2–2 draw with Everton.

Welbeck scored the only goal as Sunderland beat Bolton Wanderers on 18 December 2010, and also scored on 1 January 2011 as Sunderland defeated Blackburn Rovers 3–0. His form for Sunderland prompted widespread calls for an England call up, but on 5 January, he picked up a hamstring injury in a victory at Aston Villa, ruling him out for eight weeks. He made his return on 5 March 2011, in a 0–0 draw away to Arsenal, coming on as a substitute for Steed Malbranque in the 68th minute; he almost scored a late goal that would have won the match for Sunderland in the 83rd minute, but his shot was saved by Wojciech Szczęsny. He picked up an injury in the 4–2 home win over Wigan Athletic on 23 April, and he returned to Manchester United for treatment for the remainder of the season.

Welbeck was given a starting berth in the 2011 FA Community Shield match at Wembley Stadium on 7 August 2011. United won the match 3–2, having trailed rivals Manchester City 2–0 at half time. He started alongside Wayne Rooney in the first league match of the 2011–12 Premier League season away to West Bromwich Albion; he was substituted in the 65th minute, to be replaced by Dimitar Berbatov. On 22 August, Welbeck scored the opening goal of the match against Tottenham Hotspur, heading in a cross from Tom Cleverley from nine yards to score in the 61st minute. He then provided an assist for Anderson in the 76th minute to make the score 2–0 before being substituted. The match ended in a 3–0 win for United. Welbeck opened the scoring in an eventual 8–2 win over Arsenal. From outside the box, Anderson chipped the ball into Welbeck and he headed it over Wojciech Szczęsny. However, Welbeck had to leave the field early with a pulled hamstring which, consequently, ruled him out for several weeks.

Welbeck scored twice in a Champions League group match against Basel on 27 September; the match ended 3–3. Welbeck scored again in the next match, a 2–0 home win over Norwich City, after coming on as a second-half substitute. He exchanged passes with Park Ji-sung before sweeping low into the bottom corner to seal the win. On 21 December 2011, Welbeck opened the scoring at Craven Cottage in a 5–0 win against Fulham. He met Nani’s cross and steered the ball in with his left foot. On 8 January 2012, Welbeck scored the second goal in a 3–2 away victory against Manchester City at the City of Manchester Stadium in the FA Cup third round. Patrice Evra made a half-cleared cross, which Welbeck volleyed into Costel Pantilimon’s bottom corner. On 14 January, it was reported that Welbeck would sign a long-term contract at Old Trafford. On 22 January, Welbeck scored the winning goal in the 81st minute in a 2–1 away victory at the Emirates Stadium over Arsenal—his third goal in three matches. His impressive performances throughout the 2011–12 campaign earned him a place on the shortlist for the 2012 PFA Young Player of the Year Award, which was won by Tottenham Hotspur defender Kyle Walker.

He played in England’s deciding UEFA Euro 2012 qualifier against Montenegro on 7 October 2011, coming on as a substitute for Theo Walcott in the second half. On 29 May 2012, Welbeck was listed as a part of the confirmed 23-man squad for Roy Hodgson’s England squad for UEFA Euro 2012. On 2 June 2012, he scored his first goal for England in a 1–0 win against Belgium, with a chip over goalkeeper Simon Mignolet after collecting a through ball from his Manchester United teammate Ashley Young. On 15 June 2012, Welbeck scored a backheeled winning goal in the 79th minute as England beat Sweden 3–2 in UEFA Euro 2012 in Kiev.

Welbeck started the first match of the season against Everton on 20 August 2012, which ended a 1–0 defeat. He was substituted for the club’s new signing, Robin van Persie. On 22 August 2012, Welbeck signed a new four-year contract with Manchester United stating that playing for Manchester United is all he ever wanted. He scored his first goal of the season on 20 October, in a 4–2 win at home to Stoke City. On 13 February 2013, Welbeck scored a vital goal in a 1–1 draw against Real Madrid at the Santiago Bernabéu Stadium, heading in from a Wayne Rooney corner, his first goal in almost four months. Welbeck’s goal made him the first Englishman to score for a Premier League team at the Bernabéu since Leeds United’s Alan Smith in 2001. He ended the season with a total of two goals in 40 appearances.

Welbeck scored four goals in England’s qualification for the 2014 FIFA World Cup, braces in two home matches: a 5–0 win over San Marino on 12 October 2012 and a 4–0 victory against Moldova on 6 September 2013, He was called up for the final squad for the tournament. and started in England’s opening 2–1 defeat to Italy before being substituted for Ross Barkley after 61 minutes. Welbeck also played England’s second group match, a loss by the same score to Uruguay in which he was substituted for Adam Lallana for the last 19 minutes.

Welbeck started for United in their 2–0 win over Wigan Athletic in the 2013 FA Community Shield at Wembley Stadium on 11 August. He scored on the opening day of the Premier League season, scoring twice in a 4–1 win against Swansea City in new manager David Moyes’ first league match as Manchester United manager. On 2 October 2013, he scored his only UEFA Champions League goal of the season in a 1–1 draw with Shakhtar Donetsk at the Donbass Arena.

Between December 2013 and January 2014, Welbeck scored six goals in six Premier League matches. On 15 December, he scored twice in a 3–0 win against Aston Villa at Villa Park. On 21 December, he scored his first goal at Old Trafford since October 2012 in a 3–1 win over West Ham United. On 28 December, he scored the only goal in United’s win at Norwich City. He then scored in home matches against Tottenham Hotspur and Swansea City in January 2014.

Critics have acknowledged the strength in Welbeck’s style of play such as his work-rate, pace and intelligence in following tactical command, especially after his performance in both of Manchester United’s Champions League knock-out stage matches against Real Madrid in 2013. Welbeck has been praised as a big game player.

On 2 September 2014, in the late hours of deadline day, Welbeck joined Arsenal on a “long-term deal” for a £16 million fee. Stating the reason for his departure to a direct rival, Manchester United manager Louis van Gaal said “Welbeck doesn’t have the record of Robin van Persie or Wayne Rooney. We let him go because of Falcao, but also to allow the youngsters to fit in. That is the policy. That is why I am here.” Welbeck left Manchester United having made a total of 142 appearances, scoring 29 goals.

On 8 September 2014, in England’s first match of UEFA Euro 2016 qualification, Welbeck scored both goals in a 2–0 victory away to Switzerland at St. Jakob-Park, Basel. He then scored in matches against San Marino, Slovenia and Lithuania to make him the top goalscorer in the qualifying phase with six goals from five matches.

On 9 March 2015, Welbeck scored the winning goal to knock out his former team, Manchester United, in the quarter-finals of the FA Cup at Old Trafford. The following month, he was ruled out for the rest of the campaign with injury, missing the Gunners’ victory in the 2015 FA Cup Final.

Welbeck missed the opening weeks of his second season at Arsenal through injury, with it being announced that he would be out until Christmas with a knee injury. Around the time that he was expected to return, it was instead confirmed that he would be out until February 2016 at the earliest. Welbeck made his return on 14 February 2016 in a 2–1 win over league-leaders Leicester City as an 83rd-minute substitute, replacing Alex Oxlade-Chamberlain. He announced his return by heading in an injury time winner from a Mesut Özil free-kick. Welbeck scored in his first Premier League start of the season, Arsenal’s first in a 3–2 defeat at former team Manchester United.

After being away for eight months due to the knee injury, Welbeck was named part of Arsenal’s squad in the FA Cup match against his former club Preston on 7 January 2017. He started on the bench and entered the fray with seven minutes remaining in what was a 2–1 win for Arsenal, after Olivier Giroud scored late to give Arsenal the victory. After the match, Arsène Wenger praised the striker and said that “Welbeck can still have a dream career”.

On 28 January 2017, Welbeck made his first start of the 2016–17 season in a fourth round FA Cup tie against Southampton. He scored Arsenal’s first two goals before assisting Theo Walcott’s first in an eventual 5–0 win at St Mary’s Stadium. He started as Arsenal beat Chelsea 2–1 in the 2017 FA Cup Final at Wembley Stadium on 27 May.

Welbeck started in the 2017 FA Community Shield at Wembley Stadium on 6 August, as Arsenal beat Chelsea 4–1 penalties having drawn 1–1 after extra time. He scored his first goal of the 2017–18 season in Arsenal’s 4–3 win over Leicester City in their opening Premier League match. He went on to score twice in the team’s second home match of the season, a 3–0 defeat of AFC Bournemouth on 9 September. Welbeck picked up a groin injury during Arsenal’s 0–0 draw with Chelsea at Stamford Bridge, which ruled him out for three weeks. Welbeck ended a goalless run of 16 Premier League games to score two and assist the other as the Gunners fought back to beat Southampton 3–2.

During March 2018, Welbeck was selected for the national team for friendlies in preparation for the 2018 FIFA World Cup alongside Arsenal teammate Jack Wilshere. He was named in the 23-man England squad for the 2018 FIFA World Cup.

Welbeck signed for Premier League club Watford on 7 August 2019 on a contract of undisclosed length. Welbeck’s debut came in an away match to Everton when he came on in the 67th minute as a substitute, where Watford lost 1–0. He scored his first goal in the EFL Cup game against Swansea City where Watford won 2–1. Welbeck scored his first league goal for Watford in a 2-1 home win over Norwich City. He was released by the club on 6 October 2020.

Welbeck signed for Premier League club Brighton & Hove Albion on 18 October 2020 on a free transfer on a one-year contract. He made his debut 2 weeks later, coming on as a substitute for Leandro Trossard in a 2–1 away defeat against Tottenham Hotspur. He made his first start 5 days later, playing 86 minutes of a 0–0 home draw against fellow Premier League side Burnley.