It was a richly deserved result for the visitors, who claimed just their second win in 11 games to reclaim their place in the Sky Bet League Two play-off positions.
United controlled the game virtually from kick-off and Kitson notched the first goal of the Gary Waddock era with a tap-in just after the half hour mark.
Plymouth were poor, but Ryan Clarke was required to make two superb saves to keep out headers from Nathan Thomas and Curtis Nelson either side of half-time to preserve the lead.
They were crucial moments to keep out the hosts, who had Max Blanchard sent off four minutes into the second half after collecting his second booking.
United made the most of the extra space and Constable buried an unstoppable shot to give them a cushion.
Further chances to extend the lead came and went, but it did not prove costly as the visitors claimed a hugely important victory.
Kitson was one of four changes Waddock made to the side which started the 2-0 defeat to Fleetwood Town a week earlier.
He came in with Constable up front, as Callum O'Dowda and Nicky Wroe began in midfield.
Deane Smalley was left out of the squad altogether with a calf problem, while David Connolly, Andy Whing and Scott Davies dropped to the bench.
From the outset, the visitors looked bright in possession and played with a confidence which had not been seen for several weeks.
O'Dowda had been part of the U's side which lost an Oxfordshire Senior Cup tie at Kidlington four days earlier, but the winger had a glorious early chance to score his first senior goal.
Good work from Constable, who led the line very well, saw the striker cross for the youngster, who headed wide from close range.
It was a bad miss, but United shrugged it off to keep playing at a quick tempo.
Plymouth were forced to defend half a dozen corners in the opening 20 minutes and the home fans grew increasingly frustrated at their side's lack of influence in the game.
Kitson was the first to test Jake Cole with a well-struck shot from long range midway through the half.
The goalkeeper made a better save shortly afterwards to turn Wroe's shot round the post.
The breakthrough came just after the half hour mark and O'Dowda had a role, skinning Blanchard, who was booked for bringing the winger down.
Ruffels swung the resulting free-kick to the back post, where Ryan Williams cushioned it across goal for an unmarked Kitson to nonchalantly tap in.
It was fully deserved and United's players continued to find space deep in Plymouth's half.
The home side had hardly threatened, but they should have levelled two minutes before the break.
Lewis Alessandra crossed for Thomas, who should have buried his header, but it gave Clarke a chance to claw out the ball one-handed.
Top scorer Reuben Reid latched on to the rebound, but Michael Raynes reacted superbly to make a goal-saving block.
Plymouth's task grew tougher four minutes after the restart, when Blanchard was dismissed for pulling back Kitson.
United nearly made the numerical advantage count within minutes.
A hurried clearance from Andres Gurrieri fell to Wroe, whose shot hit the underside of the crossbar but bounced clear.
Plymouth hit back straight away and it took a breathtaking save from Clarke to keep out Nelson's flicked header which was heading for the top corner.
It proved to be a big moment in the game, as United responded to extend their lead on 63 minutes.
O'Dowda surged forward into space on the break and slipped in Constable, who unleashed a thunderbolt from 20 yards which left Cole grasping at thin air.
It was the striker's 12th of the season and took him to within one goal of equalling the club's all-time goalscoring record.
Plymouth had no option but to go for broke, stretching the game.
Gurrieri was released through on goal 19 minutes, but he shot wide as Clarke rushed out to narrow the angle.
United had chances to extend their lead as the Pilgrims increasingly took risks to get back into the game.
Wroe found Constable in space, but the striker delayed his shot to allow Durrell Berry time to make a tackle.
Williams was played through, only to scuff a shot tamely wide with only Cole to beat.
Late on Potter, brought off the bench, slid a shot just the wrong side of the post.
There was no late flourish to the scoreline, but it did not matter and with results elsewhere going their way, United returned to the top seven just a week after dropping out.
Oxford Utd: Clarke, Hunt, Raynes, Wright, Newey, Williams, Wroe, Ruffles, O'Dowda (Potter 71), Kitson (Whing 81), Constable (Davies 89).
Unused subs: Crocombe, Bevans, Rose, Connolly.
Plymouth: Cole, Blanchard, Trotman, Nelson, Gurrieri, Harvey (Showunmi 59), Wotton (Blizzard 59), Hourihane, Thomas (Berry 70), Reid, Alessandra.
Unused subs: Dawson, Boco, Morgan, Banton.
Referee: Mick Russell (Hertfordshire).
Attendance: 8,161 (451 visitors).