Walker-Peters signed for Tottenham Hotspur on 1 July 2013. In May 2015, he made his senior team debut in the post-season tour of Malaysia and Australia. In December 2015, he received Premier League Under-21 player of the month for Spurs. Wally Downes Jr reporting for The Sun Newspaper described Walker-Peters as a “brilliant 20-year-old Tottenham academy right-back” and “The teenager has all the guile of a No 10 but also the pace of a seriously nippy winger.” February 2017 saw Walker-Peters sign a new contract until 2019.
At the start of the 2017–18 season Walker-Peters made his full Premier League debut against Newcastle United helping to earn Tottenham a 2–0 away victory at St James Park. Sky Sports went on to award him Man of the Match.