Properties in the WV1, WV2, WV3 and WV6 postcode areas were affected by the leak on Wednesday.
The city's Sainsbury's superstore and the adjoining gym were also both affected.
Sainsbury's was forced to delay opening by 30 minutes, opening at 7.30am rather than 7am due to the disruption.
Residents across the city were warned to expect a drop in water pressure as a result.
Severn Trent and Wolverhampton Council closed a section of Salop Street between School Street and Worcester Street in the WV3 area as work to fix the pipe began.
The water company said it had received 37 calls from affected customers on Wednesday morning.
A Severn Trent spokesperson said: “We’re really sorry to anyone affected by the burst pipe on Salop Street, Wolverhampton.
"Our teams have identified the pipe and isolated the burst, and are working hard to get the pipe fixed and the road back to normal.
"In the meantime, the majority of supplies have been restored by moving water around the network in a different way and by using tankers to pump directly into the network.
"Again, we’re really sorry for the disruption caused, it will be our priority to make sure the pipe is fixed, with everything back to normal as quickly as possible.”
The repair in Salop Street was continuing on Wednesday afternoon, with the water company hoping to have the pipe fixed by the evening.
The Gym, on Alexandra Street, was temporarily closed in the morning but back open by the afternoon.
A statement to customers from The Gym, said: "The Gym Wolverhampton is now open following our unplanned closure.
"We apologise for any inconvenience caused during the closure and look forward to seeing you soon."
It comes less than a month since Stowheath Lane, in East Park, Wolverhampton, was flooded after a mains pipe burst. In that incident, on April 3, properties in Willenhall and parts of Walsall were also affected.