Born in Massarelos, Porto, Jota joined F.C. Paços de Ferreira's youth setup in 2013, from Gondomar SC. He was promoted to the main squad at the start of the 2014–15 season, and made his senior debut on 19 October 2014 by starting in a 4–0 home win against Atlético S.C. for the Taça de Portugal. Jota first appeared in the Primeira Liga on 20 February 2015, coming on as a late substitute for Diogo Rosado in a 2–2 home draw against Vitória de Guimarães. He scored his first goals in the competition on 17 May, netting a brace in a 3–2 home success over Académica de Coimbra and becoming the youngest player to score for the club in the top tier in the process. On 30 May 2015, Jota signed a new five-year deal with Paços, keeping him tied up until 2020. In the first game of the campaign, a 1–0 win over Académica at the Estádio da Mata Real on 17 August, he was sent off at the end for pushing Hugo Seco; Ricardo Nascimento was also sent off for retaliating on his teammate's behalf.
Atlético Madrid
On 14 March 2016, Jota agreed a five-year contract with Atlético Madrid effective as of 1 July. On 26 August, however, he returned to his country and joined FC Porto on a one-year loan. On 1 October he scored a first-half hat-trick in a 4–0 away victory against C.D. Nacional.
Wolverhampton Wanderers
On 25 July 2017, Jota moved to English Championship club Wolverhampton Wanderers on a season-long loan. He scored his first goal on 15 August, in a 3–2 away win over Hull City. On 30 January 2018, it was announced that a permanent deal with Jota had been agreed for a reported €14 million, being made effective on 1 July. He scored a career-best 17 goals in his first year, ranking fifth in the individual charts in a Premier League promotion as champions; due to English Football League regulations, he wore his legal surname on his jersey in the Championship but was able to change it to "Diogo J" after the feat. Jota made his debut in the English top division on 11 August 2018, playing the full 90 minutes in a 2–2 home draw against Everton. He scored his first goal in the competition on 5 December, helping the hosts come from behind to beat Chelsea 2–1. His second came four days later, in a win at Newcastle United by the same scoreline. On 19 January 2019, Jota netted three times in the 4–3 home defeat of Leicester City – his second career hat-trick. In the process, he became only the second Portuguese player to achieve the feat in the Premier League after Cristiano Ronaldo 11 years earlier. This was a first-ever for the club in the competition and a first for the club in the top flight of English football since John Richards, against the same opposition, in the Football League First Division in October 1977. On 25 July 2019, Jota scored in a 2–0 win over Northern Irish club Crusaders in the Europa League second qualifying round, Wolves' first European goal since October 1980, and in the next round on 15 August, he scored an overhead kick to conclude a 4–0 victory over FC Pyunik. In the final Europa League group stage game at home to Beşiktaş on 12 December 2019, Jota replaced compatriot Ruben Neves as a 56th-minute substitute with the game goalless, scored after 72 seconds and completed a hat-trick within twelve minutes as Wolves ran out 4–0 victors. The following 20 February, he netted another treble in a win by the same score over RCD Espanyol in the first leg of the last 32 of the tournament.