Walkes began his career with Tottenham Hotspur, joining the club in July 2013. He made his first team debut on 21 September 2016 in the EFL Cup against Gillingham, coming on as a substitute in the 80th minute in a 5–0 victory. Walkes appeared three times as captain in the group stage of UEFA Youth League, including twice against Bayer 04 Leverkusen. The following year, on 27 September 2017, he signed a two-year contract extension with the club, keeping him until 2019. After his loan spell at Atlanta United, Walkes returned briefly to the reserve side before being loaned out again.
Loans
On 26 January 2017, Walkes joined Atlanta United of MLS ahead of the 2017 season. Walkes made his Atlanta United debut, in the opening game of the season, coming on a late substitute but scored an own goal shortly after, in a 2–1 loss against New York Red Bulls. Initially started out on the substitute bench and his own injury concerns, Walkes quickly regained his first team place for the side, establishing himself in the right-back position. He then scored his first goal for the club on 5 July 2017, in a 4–2 win over San Jose Earthquakes. On 1 August 2017, his loan spell with Atlanta United was extended until the end of the season. He continued to regain his place for the rest of the season. Walkes then scored his second goal for the club on 14 September 2017, in a 7–0 win over New England Revolution. At the end of the 2017 season, Walkes went on to make 20 appearances and scoring 2 times in all competitions and returned to his parent club. Reflecting at his time at Atlanta United, he said his loan spell there helped push on for first team football. Walkes signed on loan for Portsmouth in January 2018. He quickly made an impact at Portsmouth when he scored on his debut, in a 2–2 draw against Doncaster Rovers on 3 February 2018. Since making his debut for the club, he established himself in the starting eleven at a right-back position. This last until in early-April when he suffered a hamstring injury that ultimately miss out for the rest of the season. Despite this, Walkes went on to make 12 appearances and scoring once for Portsmouth. At the end of the 2017–18 season, he returned to his parent club. Tottenham announced that the move to Portsmouth was made permanent on 18 July 2018.
Portsmouth
On 18 July 2018, Portsmouth announced they had signed Walkes on a two-year deal with an option on a third year for an undisclosed fee.
Atlanta United
On 9 January 2020 it was announced that Walkes would be rejoining Atlanta United of MLS, this time on a permanent transfer.
