Brophy joined UCD on a scholarship at the start of the 2005 season but found it difficult to break in to the first team and went out on loan to Kilkenny City part-way through the 2006 season.

In February 2007 John signed up with Dermot Keely at Shelbourne, initially on loan, and made his Shels debut against Kilkenny City at Buckley Park on 30 March. In May of that year he suffered a broken leg, again against Kilkenny, this time at Tolka Park, and was out for four months. He returned to action in September and made a total of 13 appearances before being released at the end of the season.

John signed for Kildare County on 3 February 2008 and made his debut for the Thoroughbreds against Shelbourne on the opening night of the '08 season. John also played with Phoenix FC in 2011/12 and in 2013/14 he was turning out with Tolka Rovers. He left to join Drumcondra for the 2014/15 season.