Exeter City Early career Watkins joined
Exeter City's academy at Under-11 level, having previously failed a trial with the club at the age of nine in 2003. He rose through the youth ranks to sign a scholarship deal in 2012. In April 2014, he signed a two-year professional contract after scoring 30 goals for the Under-18 team in its
2013–14 Football League Youth Alliance South West Conference-winning season. Watkins won his maiden first-team call up when he was named as a substitute for the final
League Two match of the
2013–14 season versus
Hartlepool United and made his senior debut when he replaced
Aaron Dawson after 77 minutes of the 2–0 victory. but despite scoring his first senior goal (a late consolation in a 3–1
Football League Trophy second round defeat to
Coventry City on 7 October 2014), he made just three appearances before departing on
loan to
Weston-super-Mare for the remainder of the season in December 2014. Through repeated extensions of the loan, Watkins would remain with the club until the end of the
2014–15 season. Watkins broke onto the substitutes' bench in October 2015 and made his first appearance of the season late in the month. His goalscoring run extended into mid-April and finished with 8 goals in 10 appearances. Watkins finished the 2015–16 season with 10 goals in 22 appearances. He had an eventful season, making 52 appearances, scoring 16 goals, and contributing 13
assists, On 9 April, he was awarded the
EFL Young Player of the Year award for his performances during the season.
Brentford On 18 July 2017, Watkins joined
Championship club
Brentford on a four-year contract, with an option for a further year, for an undisclosed fee, reported to be £1.8 million. He scored his first goal for Brentford on 8 August in their 3–1
extra-time victory away to
AFC Wimbledon in the
EFL Cup first round. On 9 August 2019, Watkins signed a new four-year contract with a one-year extension option. He scored his first hat-trick for the club in the Championship against
Barnsley in a 3–1 win on 29 September. Watkins made 50 appearances and scored 26 goals in all competitions during the
2019–20 season, which ended with defeat in the
2020 Championship play-off final.
Aston Villa 2020–2023 in 2021 On 9 September 2020, Watkins joined
Premier League club
Aston Villa on a five-year contract, for a then club-record fee of £28 million, which could rise to £33 million. Exeter City made £4 million and a further £750,000 in additional performance related add-ons from the transfer as they had inserted a sell-on clause when Watkins was sold to Brentford. In joining Aston Villa, Watkins was reunited with manager
Dean Smith, who had signed him for Brentford. On 15 September, Watkins made his Aston Villa debut, scoring in a 3–1 away win in the EFL Cup against
Burton Albion. He went on to make his Premier League debut on 21 September, in a 1–0 home win against
Sheffield United. On 4 October 2020, Watkins scored his first Premier League goals, scoring through a left footed strike, a right footed strike and a header for a
perfect hat-trick in a 7–2 home victory over champions
Liverpool. It was Liverpool's heaviest defeat in 57 years and was the first time in Premier League history that a reigning champion had conceded 7 goals in a single match. On 10 April 2021, Watkins scored against Liverpool again, becoming the first player since
Andrey Arshavin in the 2008–09 season to score as many as four goals against Liverpool in a single Premier League season. With 14 goals, he became Aston Villa's top scorer of the
2020–21 season. On 25 February 2023, Watkins scored in his fifth consecutive Premier League match, a 2–0 win away to
Everton, becoming the first Aston Villa player to achieve this feat.
2023–present On 23 August 2023, Watkins scored a hat-trick in Villa's 5–0 win against
Hibernian in the
2023–24 UEFA Europa Conference League play-off round, which ensured the team's qualification for the group stage. On 30 September, he scored his second hat-trick of the
2023–24 season and his third for Aston Villa in a 6–1 home win over
Brighton & Hove Albion. On 6 October, Watkins signed a new contract with Aston Villa, committing his future to the club until 2028. On 14 April 2024, he scored a goal in a 2–0 away win over
Arsenal, in which he became the joint-top scorer for Aston Villa in a single Premier League season, 19 goals without penalty kicks, equalling
Christian Benteke's record in 2012–13. On 14 May 2024, at Aston Villa's 2023–24, Watkins was voted Supporters' and Players' Player of the Season. At the end of the season, Watkins won the
Premier League Playmaker of the Season award for the most
assists of the season, with 13. Watkins was also named in the Premier League Fan Team of the Season. Watkins' first goals of the
2024–25 season season came in a 3–2 home win against
Everton in the Premier League, with Watkins scoring twice in the second half to earn him the Man of the Match award. On 29 January 2025, he scored his first
UEFA Champions League goal, provided two assists and missed a penalty in a 4–2 victory over
Celtic. Watkins scored after 30 seconds against
Newcastle United on 19 April, a game Villa went on to win 4–1. This put him on 74 Premier League goals for Villa, drawing him level with
Gabriel Agbonlahor for most goals in the league for the club. On 10 May, he broke the previous record, scoring his 75th goal for Villa in a 1–0 away win over
Bournemouth. In November 2025, Aston Villa manager
Unai Emery announced that Watkins was one of Aston Villa's deputy captains, behind captain
John McGinn and vice captain
Ezri Konsa. A month later, on 27 December, he netted a brace in a 2–1 away win over
Chelsea, helping his team secure an 11-match winning streak that matched club records previously achieved in September 1897 and March 1914. On 16 April 2026, Watkins scored his 100th Aston Villa goal during a 4–0 Europa League
quarter-final victory over
Bologna, becoming Aston Villa's joint 10th all-time goalscorer and their all-time top European goalscorer. ==International career==