Ryan Hawkins played for a young Norwich City Under-18s against Manchester City on 30th April 2013, which the Canaries lost 4-1. Most of their Under-18s were rested for the FA Youth Cup final. He had been with Norwich's academy at the age of seven. He played for Dereham Town, making his debut aged 16,before joining St Neots Town in May 2015. In January 2016, he trialled with Peterborough.

In the summer of 2016, he trialed with league side Stevenage whilst it was understood another League Two club and a League One outfit after also tracking the attacking ace, Joint St Neots boss Andy Davies said: “We’ve had interest in Ryan from two or three clubs, but Stevenage are the first to have taken it a step further. There is no doubt in my mind that he has the ability to play in the Football League. He has quality on the ball, good movement off it and the sheer pace to be a success at that sort of level. We are a club which likes to unearth, develop and promote young talent. Ryan is under contract so there will be a fee involved in any move, but we won’t stand in the way of a young player with a chance to progress in the game.”

Hawkins trialled with Newport County in October 2016 whilst studying at the University of East Anglia and was linked in November 2016 with a move to Kings Lynn Town. He eventually signed for the Linnets on 16th November 2016 for a four figure sum rumoured to be £2,250.

In August 2019, he returned to Dereham on a two month loan

On 17th June 2020 it was confirmed that Lynn were winners of the National League South, on a points per game basis due to the premature ending of the season because of Covid-19, and would be promoted into the National League.

On 23rd October 2020 it was announced that Hawkins has left Kings Lynn with his contract cancelled. Director of Football Rob Beck said "Ryan has been a good servant to the football club in his time here and has been involved in some remarkable days with the team. There aren’t too many players who are able to say they have been part of a team that has achieved back-to-back promotions, but Ryan is one player who can do that. He has always given the club full commitment and effort in his time here. On behalf of everyone at the club, I would like to wish Ryan well for the future, both on and off the pitch and he will always be most welcome at the club in the future.”.

Hawkins then signed for Southern League side Lowestoft on 31st October 2020 signing a two year deal. Trawlerboys manager Jamie Godbold admitted Hawkins was a player who had been on his radar for “a number of years” and he had previously tried to sign him when he was manager at AFC Sudbury, but back then he joined King’s Lynn. He said “I am delighted to be able to bring Ryan to Lowestoft and that he has accepted our offer amongst other interest. He is more than proven at our level and if you look at his last four to five years he has been involved in teams at the top end of the divisions they’ve been in, so he knows what it takes, he is a winner.I have managed teams that have played against Hawks and he causes you problems."

During the 2021/22 season he signed for Peterborough Sports.

He joined Wroxham in June 2022.