The win on Monday (Tuesday AEDT) was a real boost for Coventry, who had lost their first four games of the season but edged past Nottingham Forest in the final league match before the international break.
The victory also marked their first in the Premier League in 25 years after the Midlands club returned to the top division this season.
Cherif was brought down just four minutes into the game and Jack Rudoni made no mistake from the spot.
Newcastle controlled most of the first half without troubling the Coventry goal, but it was a different story in the second period as the home side won the game with some clinical finishing.
Cherif made it 2-0 with a low shot from the edge of the box three minutes into the second period, and although Sven Botman reduced the deficit with a stunning strike in the 70th minute Ellis Simms restored the two-goal advantage nine minutes from time.
Stephen Mfuni, the 18-year-old centre half on loan from Manchester City, scored his first professional goal in the 86th minute to cap a dream night for Coventry and lift Frank Lampard's men into 14th place.
"It is so hard to win, but we played like the team we want to be tonight," Lampard said.
"We know we are going to have to suffer a lot in games this season, but the work ethic of the boys and the belief mean you get what you deserve."
Newcastle are three places and two points above them, and coach Matthias Jaissle warned he had work to do after a second straight 4-1 loss away from home following a similar result at Leeds a month ago.
"Back-to-back 4-1 defeats away are things we need to avoid in the future," he said.
In a touching sidenote, Coventry midfielder Rudoni dedicated his goal to his grandmother, who is in hospital after suffering a heart attack last week.
The 25-year-old stepped up for the penalty after Cherif was felled by goalkeeper Lukas Hornicek and calmly slotted into the bottom right corner to give Coventry an early lead.
Rudoni wheeled away to celebrate his first goal of the season and lifted his shirt up with a message that read "Get well soon Nan''.
After the match he told Sky Sports: "Last week, she unfortunately had a heart attack. She's stable, she'll be watching this from hospital and she's a strong woman so she'll definitely come through.
"That one was for you, Nan. I just wanted to dedicate it to her watching it in hospital."
- with PA
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