Jake Cain was at the Liverpool Academy since the age of nine and signed his first professional contract in 2019. The central midfielder made his first team debut in the FA Cup 4th round replay win against Shrewsbury.

During the 2020/21 season, Cain was an unused substitute in nine of Liverpool's ten Champions League games and two in the Premier League. For the Under 23's he scored six goals in 23 appearances in Premier League 2. In August 2021 a season long loan deal was agreed with League Two side Newport County, where Cain made 28 appearances in all competitions. He remained with Liverpool's under 21's for the first half of 2022/23, but moved to Swindon of League Two in the January transfer window for an undisclosed fee, signing a two and a half year deal. He was released at the end of 2024/25, having fallen out of favour under Mark Kennedy and then failing to convince new manager Ian Holloway that he was worthy of a new contract.