Walker had to come off the bench and don the gloves after substitute goalkeeper Claudio Bravo was sent off for a last-man foul on Josip Ilicic in the 81st minute.
The defender's first action was to save the resulting free kick — although not without spilling it onto the ground before scooping up the ball.
"I try and sometimes (wind up) the other keepers in training, telling them to catch it," Walker said. "But as I found tonight, sometimes you do have to take two touches."
He didn't have much more to do, though, as City managed to see out the final minutes.
The Italian side looked headed for a fourth straight loss in Group C when Raheem Sterling — who scored a hat trick in Man City's 5-1 win in the reverse fixture — put the Premier League champion in front in the seventh minute.
However, Gabriel Jesus dragged a penalty wide three minutes before halftime and Mario Pasalic leveled for Atalanta four minutes into the second half.
Atalanta dominated the second period and its winning chances increased when Ilicic burst through clear on goal and was brought down by Bravo, who had come rushing out of the area.
With Bravo having come on as a halftime replacement for the injured Ederson, Pep Guardiola had to put Walker in goal.
Sterling posted a photo on Twitter of him and Walker — dressed in Bravo's goalkeeping jersey — laughing on the pitch after the game, but added: "I wouldn't trust you holding my baby tho."
City remained top of Group C and five points clear after Shakhtar Donetsk scored two late goals to draw 3-3 at Dinamo Zagreb.
"We have to take our hats off to Atalanta. You know as well as I do what a good side they are," Guardiola said. "You can ask all Italian teams just how hard it is to face Atalanta. To take four points off them is a big success for us, especially with the injuries we've faced. We played well in the first half then dug deep in the second."
Atalanta stayed bottom of the group, four points below Dinamo Zagreb and Shakhtar with matches against both still to play.
"At the end maybe we could have got more, especially after they had a player sent off, but we got a point and we're still in it," Pasalic said. "We're looking ahead. If we play the next two matches like we played the second half today we can go good things. It's down to us."
City would have secured a spot in the knockout round with a win and took an early lead with a delightful move. Bernardo Silva played in a ball from the left and Jesus backheeled it into the path of Sterling, who slotted into the bottom corner.
Sterling had numerous chances to add to his tally but he just failed to connect with a cross from Riyad Mahrez and then had a shot blocked by Hateboer.
City was awarded a penalty shortly before halftime but video review showed that Rafael Toloi's shirt tug on Sterling was outside the box and a free kick was given instead.
However, Sterling's free kick then hit Ilicic's hand in the wall and, after reviewing it on the pitch-side monitor, referee Aleksei Kulbakov awarded a penalty.
But Jesus hit a tame effort wide of the right post. City then suffered a blow ahead of Sunday's key Premier League game with Liverpool as goalkeeper Ederson had to go off at halftime.
Bravo's first action was to pick the ball out of the back of the net after Pasalic was left unmarked to head in a cross from Alejandro "Papu" Gomez.
That appeared to boost Atalanta's confidence and it went close to taking the lead on several occasions, notably when Berat Djimsiti headed a corner just wide of the left upright.