Hughes and Molesley both put in assured performances, alongside a number of players from the development squad, in front of management duo Paul Groves and Shaun Brooks.
The Cherries were in control for large periods of the game and created more chances, but Jack Evans’ goal ten minutes from time earned the Gills the win.
Chris Hargreaves’ side went close on a number of occasions and striker Jordan Chiedozie hit the woodwork three times before the visitors took a late lead.
First Chiedozie struck the bar with a spectacular overhead kick, then saw his shot rebound off the post after being played in by a fine through ball from Harrison Gilkes.
Goalkeeper Chad Collins, who had been named on the bench for the first two first team games of the season, had a quiet afternoon but made a great reaction save to keep the scores level at the interval.
Chiedozie was frustrated again early on in the second half as his shot clipped the top of the bar, while Jayden Stockley also tested the Gillingham goalkeeper.
Collins was beaten in the dying stages as Evans smashed the ball past the Cherries ‘keeper from an indirect free-kick inside the penalty area.
Cherries: Collins, Case, Bowles (Gregory, 45), Strugnell, Cargill, Moth (Bussell, 52), Jamal (Wilson, 52), Molesley (Hughes, 45), Gilkes, Stockley (Saadi, 78), Chiedozie (Makoni, 52).