Ben Seymour's 71st minute penalty gave the visitors the lead, but Dewsbury-Hall's tidy late equaliser stretched Leicester's unbeaten run to seven matches in all competitions.
There were four changes to City’s starting XI after Monday’s brilliant Premier League 2 success at Swansea City, where the Club’s youngsters ran out 3-0 victors.
In came goalkeeper Max Bramley, midfielder Khanya Leshabela and attackers Ryan Loft and Conor Tee, replacing Viktor Johansson, Lamine Kaba Sherif, Ali Reghba and Admiral Muskwe.
Both sides struggled to command the opening 45 minutes, however, with seven of the Foxes stars who appeared in Swansea 48 hours earlier once again in action.
On a bitterly cold evening in Whetstone, Leicester were as dogged and determined as ever, but found an organised Exeter rear-guard blocking their route to James Hamon’s goal.
Loft, who spent a loan spell with the Grecians last year, gave City a man to aim for in attacking positions, while Tee, the 2017/18 Academy Player of the Season, also added guile up front.
However, the first real opening of the game fell Exeter’s way in the 52nd minute as Bramley leapt across his line to palm a Jimmy Oates header behind for a corner.
Moments later, Joel Randall skipped into the Foxes’ penalty area and played in Jordan Tillson, who tried to poke it goalwards, but Bramley was there once again to keep it out.
The visitors got their reward for a sustained period of pressure with 69 minutes on the clock as Seymour was felled in the area by Alex Pascanu.
Seymour duly stepped up to take the spot-kick, sending Bramley the wrong way and firing it into the bottom right corner.
It was becoming a frustrating evening for the Foxes - until Dewsbury-Hall pounced to finish a well-taken goal from the edge of the area in the 83rd minute to rescue a precious point.
Who impressed?
Kiernan Dewsbury-Hall continues to be an important figure for the Club's Under-23s, scoring the goal his performance deserved on Wednesday night.
The central midfielder was again in impressive form for the Foxes, despite the tough circumstances, playing 48 hours after his most recent outing.
Where does it leave us?
Ending the night where they started it, Leicester remain second in Group D, with one win and draw to their name, five points adrift of Nottingham Forest, who have won all three of their matches so far.
Now at the half-way stage of the group stage campaign, all the sides will play each other at alternate venues to determine who finishes in the top two qualification berths.
Coming up…
City’s Premier League Cup campaign continues with a trip to Norwich City’s training ground on Monday evening (7pm GMT kick-off).
The details…
City: Bramley, Johnson, Ughelumba, Dewsbury-Hall, Knight, Pascanu, Wright (Martis 78’), Leshabela, Loft, Shade (Muskwe 72’), Tee (Kaba Sherif 69’)
Subs not used: Thomas, Davies
Goal: Dewsbury-Hall 83'