Rev Rose Hudson-Wilkin, who is also a chaplain to the Queen, will take up her new post as Bishop of Dover in November.
The Archbishop of Canterbury, Justin Welby, welcomed the appointment, saying Jamaican-born Rev Hudson-Wilkin was "one of the most influential and effective ministers in the public square".
"I am absolutely delighted that she is willing to be the new Bishop of Dover," he said.
Rev Hudson-Wilkin was the first female Speaker's chaplain and the first from a minority background when she joined the Commons in 2010.
She conducts the daily prayers in the Commons chamber, takes part in the Speaker's procession and provides pastoral care for MPs and staff in the Palace of Westminster.
Mr Bercow said: "Rose is one of the warmest, kindest and most loving people I have ever met, so she will be sorely missed by Members across the House, the staff, and especially by me.
"She has an unfailing sense of duty and an ability, more than she would herself ever know, to bring comfort in times of tragedy.
"Furthermore, her steely resolve when confronted with loss and evil, following the death of our dear colleague Jo Cox, and in the wake of the Westminster Bridge attack, was plain for all to see.
"Both in the celebration of happiness and in condolence and prayer, she has the most reassuring, fortifying presence anyone could want.
"Personally, I would like to thank Rose for her steadfast support and friendship over the last nine years.
"Our loss is certainly the Diocese of Canterbury's gain. She will be an excellent Bishop of Dover, and I will watch keenly the next stage of her spiritual journey."
Rev Hudson-Wilkin said: "I have loved every minute of being the Speaker's Chaplain - I describe it as walking in a slice of history.
"Mr Speaker has been the most amazing colleague and friend - he has been very supportive, a great encourager and I am particularly saddened to be leaving him and his wonderful team.
"However, I am equally excited about my new role and the opportunity to work with the Archbishop of Canterbury as the Bishop of Dover."
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