The stand-in captain finished off a goalmouth scramble 11 minutes from time to give Gills their third successive victory which catapulted Mark Stimson's side to a season-high fourth place.
It broke Exeter's stout resistance, but they were made to pay for a lack of ambition going forward which invited pressure from the home side.
Fresh from away wins against Morecambe and Port Vale in the previous seven days, Gillingham began brightly without creating any clear chances.
Exeter, who had a good win on the road of their own in midweek against Dagenham & Redbridge, almost took the lead with their first effort of the game on 14 minutes.
Neil Saunders floated a speculative chip from 20 yards which almost embarrassed goalkeeper Simon Royce, rebounding off the crossbar to safety.
The woodwork came to Exeter's rescue five minutes later, when Nicky Southall curled a free-kick which smacked the crossbar in an otherwise low-key first half.
Gills emerged from the interval with renewed vigour, but struggled to prise open a well-organised Grecians defence. When they did get a chance they found goalkeeper Paul Jones in good form.
But only Liverpool and Manchester United have longer unbeaten records at home in the league this season than Gillingham's 11-game run and eventually their pressure told.
John Nutter's cross was flicked high into the penalty area by the excellent Dennis Oli. Simeon Jackson scuffed a shot but the rebound fell to Miller, who tapped home for his second goal in as many games.
Exeter only managed one effort on Royce's goal in the second half and, despite a late flurry, never looked like getting back into the game.