[11][12] In Round 21, Holmes made his NRL debut for Cronulla-Sutherland against the Parramatta Eels on the wing in the 32–12 loss at Remondis Stadium filling in for Sosaia Feki who succumbed to an injury before the match.
[20][21] In Round 10 against the Gold Coast Titans, he kicked a field goal to win the match for Cronulla in their 23-22 golden-point extra-time victory at Cbus Super Stadium.
[22] In Round 19 against the Canberra Raiders, he repeated his efforts, kicking another field goal in extra-time to win the match 21-20.
In round 12 of the 2018 NRL season against the Newcastle Knights, Holmes scored a hat trick of tries in Cronulla's 48-10 win at Hunter Stadium.
[32] On 24 November 2019, Holmes returned to rugby league, signing a six-year deal with the North Queensland Cowboys, beginning in 2020.
[35] In his second game back from injury, a 16–42 loss to the Sydney Roosters, Holmes reinjured his ankle and missed seven weeks.
[37] In Round 17, Holmes kicked the winning field goal in golden point to defeat the St. George Illawarra Dragons 23–22 and snap North Queensland's nine-game losing streak.
In round 9 of the 2021 NRL season, Holmes kicked the winning field goal for North Queensland as they defeated arch-rivals Brisbane 19-18.
He was named on the wing before an injury to Kalyn Ponga forced him into the fullback role for the 50-6 loss to New South Wales.
[44] In round 19, Holmes kicked a penalty goal after the siren to win the match for North Queensland against the Wests Tigers by 27–26.
[46] In the 2022 Qualifying Final, Holmes kicked a two-point drop goal in extra-time as North Queensland defeated Cronulla-Sutherland 32-30.
In round 17 of the 2023 NRL season, Holmes scored two tries and kicked five goals as North Queensland upset South Sydney 31-6.
[52] On 10 September 2023, Holmes became the subject of investigations by the NRL Integrity Unit and the North Queensland Cowboys after posting a photo to his Instagram showing himself with a white bag in his mouth.
[53] On 13 September, Holmes was issued a breach notice by the NRL for allegedly bringing the game and his club into disrepute.
[54] In round 12 of the 2024 NRL season, Holmes scored two tries and kicked six goals for North Queensland in their 42-28 victory over strugglers the Wests Tigers.
On 15 August , Holmes signed a three-year deal with the St. George Illawarra Dragons starting in the 2025 NRL season.
[56] In April of 2019, Holmes was signed by the New York Jets as part of the NFL's International Player Pathway program.