In November 2016, Slater made his first team debut against Grimsby Town; scoring a goal in the 4–2 victory and becoming the youngest footballer to achieve this feat for the club.[7] On 28 December 2016, Slater was promoted to the senior team; penning a deal which would keep him at the club till 2020.[8]
On 16 December 2017, Slater made his league debut, replacing Samir Carruthers in a 1–0 defeat against Preston North End. In January 2018, he made an appearance against Ipswich Town in the FA Cup; where his tackle against Bersant Celina was later said by manager Chris Wilder to be his "personal highlight" of the match.[6]
On 20 July 2018, Slater was loaned out to League Two club Carlisle United on a one-year deal.[9] He scored his first two goals for the club in a 4–0 win over Swindon Town in November 2018.
On 27 July 2019, Slater signed a season-long loan with Scunthorpe United, the same day scoring on his debut in a pre-season friendly against Lincoln City.[10][11]
On 30 September 2020, Slater signed a season-long loan with Hull City.[12] He made his debut on 3 October 2020 in the home win to Plymouth Argyle.[13] On 27 October 2020, he came off the bench in a triple-substitution, away to Bristol Rovers and scored the second goal for Hull in a 3–1 win.[14]
On 27 January 2022, Slater returned to the Hull City after signing a two-and-a-half-year deal for an undisclosed fee,[15]
revealed to be £50,000.[16]
On 2 May 2023, Slater received both the Player's Player and Supporter's Player of the Year awards following his strong 2022–23 campaign.[17]
On 21 June 2023, Slater signed a new three-year deal with Hull City.[18]