Born in Enfield, Onomah came through the academy system at Tottenham Hotspur. He was first called up for the first team on 5 January 2015, remaining an unused substitute in their 1–1 draw away to Burnley in the FA Cup third round, and made his debut nine days later in the replay, replacing Andros Townsend for the last 15 minutes of a 4–2 victory at White Hart Lane. On 24 May, he was included in the matchday squad for a Premier League game for the first time, remaining unused as Tottenham won 0–1 at Everton in the last game of the season.
In the 2015–16 season, Onomah changed his shirt number to 25, which was included on the club’s list of first-team numbers. He made his Premier League debut in a 3–1 home victory over Aston Villa on 2 November 2015, replacing Dele Alli for the final minutes. On 10 December, Onomah made his first start for Tottenham playing 90 minutes in a 4–1 victory over AS Monaco.