Derry suffered their first Eircom Premier Division defeat of the season at the Carlisle Grounds.
Gerard Doherty saved from Bray's Ger Rowe while Derry defender Stephen Gray twice went close with headers in the first half.
City striker Conor Sammon was denied by Derek Pender's goalline clearance just after the break.
Alan Cawley scored the only goal from a 75th minute penalty after Clive Delaney was sent-off for hauling down Rowe.
Derry still threatened despite being a player short and Wanderers keeper Chris O'Connor made a good save from Niall McGinn.
Gareth McGlynn failed to make contact with a late cross as Bray held on for their second win of the campaign.
The Candystripes remain second but they have slipped four points behind leaders St Pat's, who beat Cobh Ramblers 1-0 at Richmond Park.
Elsewhere, Cork secured a 3-0 home victory over Finn Harps and Shamrock Rovers drew 1-1 with UCD.
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