Hawks can have few complaints about the result as only keeper Ross Worner saved them from a much bigger defeat.
The match was only arranged with 48 hours notice and Boro boss Danny Bloor confessed he was ‘not best pleased’ when told league officials his club had to cross the Sussex-Hampshire border.
But it was Bloor who wore a wide smile at the end following a performance which left the few people in the ground wondering how they had only won one of their previous seven games and exited the FA Trophy at lower division Haringey.
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Hawks looked very uncomfortable at the back right from the off and could have been behind long before Whelpdale slid in to convert a low Charlie Kendall cross on 35 minutes.
Sub Charlie Lambert - on for the injured Charlie Walker, yes Eastbourne are a real bunch of Charlies, aren’t they! - should have doubled the advantage 60 seconds later. After Worner had dived to beat out a Kendall shot, Lambert had the goal at his mercy but his shot clipped the top of the crossbar.
Hawks boss Paul Doswell was forced into a tactical change shortly after, withdrawing right back Christian Rowe and putting on striker Danny Kedwell.
Rowe had been given a torrid time by the pacy Greg Luer, and it was no real surprise to see him taken off with Roarie Deacon moved to right back.
Doswell made another change at the interval, taking off midfielder Leon Chambers-Parillon - struggling after testing positive for Covid - and putting on winger Daniel Ajakaiye.
Hawks levelled on 57 minutes with their first on-target effort of the game.
Their only worthwhile passing move of the game ended with Tommy Wright picking out Bedsente Gomis’ well-timed run and the midfielder sidefooting home from 12 yards.
Hawks instantly started playing with more confidence, knocking the ball around confidently for the first time in the match.
But it was Eastbourne who restored their lead on 66 minutes when Lambert dinked a teasing cross to the edge of the six-yard box which Whelpdale headed back across Worner and into the bottom of the net for his 11th goal of the season.
Whelpdale was twice denied a hat-trick by Worner.
The keeper first dived to his left to push a low shot aside for a corner, after Kendall had created the opening with some direct running, and then producing an even better stop when the attacking midfielder had a clear sight of goal 10 minutes from time.
Hawks ended with four attackers on the pitch - Joe Iaciofano their third sub to go alongside Wright, Kedwell and Ajakaiye.
Moussa Diarra was also thrown up front late on, but the nearest Hawks came to an equaliser they didn’t really deserve was when Kedwell headed a corner over.
Tommy Wright was given barely a sniff of goal all afternoon by impressive centre half pairing Mitchell Dickenson and Steven James - Borough’s defensive showing a total opposite to the gaps freely on show in the home back four.
With four minutes of time added on, Hawks won a free-kick 25 yards out - but Kedwell fired his effort wastefully high and wide.
It summed up Hawks’ afternoon. The quality of their set-pieces had been a big factor in the win against Hungerford a fortnight earlier, but here Josh Taylor’s corners and long throws were rarely remotely a threat.
From either set pieces or open play, and up front and in defence, Hawks had struggled throughout
‘We got ourselves back into it with a great goal, but in the context of the game it was our one great play,’ said Doswell.
‘We then gave away a soft goal and we never really recovered.
‘You have to give credit to Eastbourne - their front three caused us all sorts of problems.
‘Whelpdale was the best player on the pitch by a mile.’
Doswell added: ‘(Craig) Robson, Gomis and (Godfrey) Poku were our three better players. I’ve said before if you don’t get eight or nine of your team at their level … and to be fair very few of our team hit their level.
‘It was an average to poor performance from about seven of the team.’
Hawks have now dropped out of the NL South play-off zone, though still with numerous games in hand on the teams above them.
Hawks: Worner, Straker, Rowe (Kedwell, 38), Diarra, Robson, Poku, Gomis, Taylor (Iaciofano, 72), Chambers-Parillon (Ajakaiye, 46), Deacon, Wright.
Eastbourne: Ravizzoli, Rollinson, Innocent, Ferry, Dickenson, James, Kendall, Hammond, Luer, Walker (Lambert, 23), Whelpdale.