The result leaves the Rustics in second place in Southern Counties East League Division One, one point behind leaders Kennington, in their bid to return straight back to the top flight.
The crowd of 121 at Jockey Farm was more than double any other game in the division and only two Premier Division games attracted higher attendances.
With their strikers Reuel Powell-Downey and Luke Adams – on 35 goals between them – both out injured, Rusthall were forced to make tactical changes with Charlie Clover playing on his own up front.
Rusthall got off to a strong start, putting the visitors under pressure, and on seven minutes a clumsy challenge saw the home side awarded a penalty.
With regular penalty-taker Adams unavailable, Tommy Lawrence stepped up to calmly send the keeper the wrong way.
But rather than building on early lead, Rusthall became sloppy with their passing and invited Sutton to get a foothold in the game.
Arlie Desanges, Sutton’s hugely experienced striker, was causing problems with his movement and home keeper Billy Johnson had to be at his best to keep him out on 21 minutes.
In the second half Rusthall continued to struggle to hold onto the ball, but despite their early pressure Sutton never really created a clear-cut opportunity.
On 69 minutes the Rustics made a fine break down the right and a driven cross allowed substitute James Miles to drill home at the far post and make it 2-0.
Louis Clarke, who has been out injured for three months, came on as a substitute and the pacy winger soon showed what the Rustics have been missing.
Sutton were still working hard and set up a tight finish on 69 minutes when Desanges finished in style following a good build-up down the left.
This seemed to shock the home side into a response and they went in search of the goal that would make the game safe.
It finally came on 84 minutes when Clarke embarked on a mazy run wide on the right and cut inside before sliding a perfect ball across the box for Miles to finish well.
Then in added time Clover unleashed a thunderbolt from just inside the box and the ball flew into the top left-hand corner.
With several players carrying knocks, manager Jimmy Anderson is looking to add some new faces to the squad as they head into the business end of the campaign.
Rusthall now have three away games, starting with Lewisham Borough on Saturday (February 8, kick-off 3pm) before taking on promotion rivals FC Elmstead and Holmesdale.