Siphosethu Ndlabi scored the only goal of with a 23rd minute penalty at Athlone Stadium on Tuesday.
Milford can now take a break this weekend as City travel to Polokwane to face Magesi at the Seshego Stadium on Saturday. They are next in action against Magesi on Wednesday.
Having entered the play-offs as underdogs, Pupuma admits that their promotion hopes lie in their hands, with two home fixtures to come, after a morale-boosting away win over City for a massive three points.
Pupuma explained that playing at home gives the team a real chance of a win in their next fixture.
"We know that the game against Magesi FC will be a tough encounter, but we are banking on the fact that it's a home game and our record at home is very good," he said on IOL.
"As for the mental side, we as a team still have the same goal as we did at the beginning of the season — and that is to gain promotion to the Betway Premiership.
“We just need to be grounded and focused as a team and also keep the boys focused on the task at hand. The win against Cape Town City gave us a massive boost, but the job is not yet done and we have to stay focused.”