Ingham started his career with Olympic FC seniors in the National Premier League while training to be an electrician. In July 2013, he was picked as one of Australia's top eight players outside the A-League. Selected in the QLD NPL football team of the year 2013.
Brisbane Roar
At the beginning of the 2013–14 National Youth League, Ingham joined Brisbane Roar's youth side. Scoring 13 goals in 11 appearances. Including a second half hat-trick that secured victory over Adelaide. On 24 January 2014, Ingham debuted for the senior team, coming on as a substitute in the 72nd minute of a 2–1 victory over Wellington Phoenix.
Ingham trained with Melbourne Victory for a month ahead of the 2016 January transfer window and was signed as the club's first use of the Mature Age Rookie salary cap allowance. Ingham made his debut for Melbourne Victory against the Central Coast Mariners on 8 January 2016, coming on as a 77th-minute substitute for Fahid Ben Khalfallah in an eventual 3–3 draw. Ingham made his first start for Melbourne Victory in their opening 2016 AFC Champions League match against Shanghai SIPG F.C. on 24 February 2016, in what was only his third appearance for the club. During the match, he scored his first goal for the club, scoring in the 31st minute in an eventual 2–1 win. He then went on to make his first A-League starting appearance on 6 March against the Central Coast Mariners, setting up both Besart Berisha and Fahid Ben Khalfallah for goals and was voted best on ground in a 2–0 win at Central Coast Stadium. Ingham scored the equaliser against Juventus F.C. in a pre-2016–17 A-League season friendly match at the MCG. Ingham scored his first A-League goal for Melbourne Victory on 12 November 2016, against the Western Sydney Wanderers, in an eventual 3–0 win. Ingham has an impressive AFC Champions League record for Melbourne Victory with 9 appearances 3 goals and 1 assist. Due to this Fox Sports commentator Andy Harper gave him the nickname "The Asian Specialist," after his third goal in Asian Champions League against Chinese giants Guangzhou Evergrande, April 22nd 2019. Ingham was released by Melbourne Victory at the conclusion of the 2018–19 A-League season.
Central Coast Mariners
In June 2019, Ingham joined Central Coast Mariners on a two-year contract among a host of signings under new coach Alen Stajcic.
Return to Brisbane Roar
In August 2019, less than 2 months after signing with Central Coast Mariners, Ingham negotiated a mutual contract release with the club and joined Brisbane Roar.
Jai is the cousin of Samoan international Johnny Hall and brother of Perth Glory player Dane Ingham. In addition to holding an Australian passport, Ingham also holds Samoan and New Zealand passports, as he has a Samoan-New Zealand mother and an Australian father.
