A late goal again proved costly on the road for Town as Jack Sparkes' odd goal out of seven ensured Exeter twice came back from two goals down to claim all three points.
Luke Armstrong and Jack Muldoon had put Town 2-0 up, with a soft penalty decision allowing Jevani Brown to reduce the deficit before the break.
George Thomson headed home in the 64th minute, but much like at Rochdale on Saturday, Town couldn't hold on to three points with Jonathan Grounds and Timothee Dieng pulling them back on level terms in the second half.
Sparkes then provided a finish worthy of winning such an entertaining contest, cutting inside from the left and curling into the roof of the net with the outside of his boot.
Simon Weaver made two changes from Saturday's point at Rochdale as Muldoon returned to the starting XI alongside Will Smith, who made his first start since October, on loan duo Josh Austerfield and Brahima Diarra making way.
Town took the lead after just four minutes as Armstrong netted his first goal since Tuesday 4th January, taking a touch to control Jack Diamond's low cross before calmly finishing.
Mark Oxley was called into action not long after, showing his one-on-one ability to deny Matt Jay who was baring down on goal.
Town doubled their lead in the 19th minute when Josh Falkingham turned a cleared corner back towards goal that Leon Legge tried to flick in, though the ball fell to the feet of Muldoon who gladly dispatched his 11th of the season.
Such was Town's dominance, Exeter Manager Matt Taylor opted for an early change, replacing Cheick Diabite with Josh Coley in a move that swung the tie in the hosts favour.
Town again had Oxley to thank for keeping Exeter out, after pushing Smith's looping header up onto the bar, Town's number one twice got in the way of efforts from Sam Nombe and Jay who had looked destined to score from a yard out.
The hosts had improved since the change, but were fortunate to be given the chance to pull a goal back from the spot in the 37th minute as Warren Burrell conceded a penalty, despite looking to have played the ball.
Town responded well to the setback with a late counter attack falling to Lewis Page, though the former Exeter man couldn't slide the ball past Cameron Dawson and Town were sent into half time with a one goal advantage.
Alex Pattison nearly restored Town's two goal advantage in the 54th minute as he met Thomson's corner with his head, only for Dawson to tip the attempt onto his own post.
Rather than swinging the next one in for his teammates, Thomson got on the end of Town's next corner, drifting in at the near post to get his head to Page's delivery and put his side 3-1 up after 64 minutes.
Another set piece ended up in the back of the net six minutes later, in Exeter's favour this time as Jonathan Grounds turned the ball goalwards after it was only partially cleared, with Brown causing Oxley a nuisance on the line.
The chances kept falling at both ends, though Diamond couldn't add his name to the scoresheet after both Armstrong and Muldoon had headed the ball on into the forward's path, slding agonisingly past the post.
Town would rue the missed chance as Exeter pulled themselves back on level terms for the first time since the fourth minute as Jake Caprice's cross was guided past Oxley by the head of Dieng.
The hosts claimed all three points deep into second half stoppage time as the ball was worked to Sparkes on the left, who cut inside Thomson before curling into the roof of the net with the outside of his boot.
Town: Oxley, Page (Austerfield 89), Falkingham, Smith, Burrell (Sheron 83), Thomson, Pattison, Muldoon, Legge, Diamond, Armstrong
Subs not used: Beck, Cracknell, Kerry, Diarra
Goals: Armstrong 4, Muldoon 19, Thomson 64
Booked: Diamond, Armstrong
Exeter: Dawson, Caprice, Sparkes, Atangana (Dieng 45), Stubbs (Grounds 52), Jay, Collins, Nombe, Brown, Sweeney, Diabate (Coley 26)
Subs not used: Brown, Amond, Key, Taylor
Goals: Brown 37 (p), Grounds 70, Dieng 81, Sparkes 90+5
Referee: B Huxtable
Attendance: 3,852 (37 away)
Atangana (Dieng 45)
Stubbs (Grounds 52)
Diabate (Coley 26)
Page (Austerfield 89)
Burrell (Sheron 83)