The politician remained stony-faced as she was berated by the leader of rank-and-file police officers over her handling of police pay, and ridiculed about her drug-taking history.
Police Federation chairman Jan Berry accused the Home Secretary of "betraying" the police service.
As the two women shared a stage at the federation's annual conference, Mrs Berry said: "Your recent crimes have been more for the serious fraud office than the drug squad."
The Home Secretary looked uncomfortable as she faced 1,000 delegates, at first smiling at the comments but her expression soon becoming rigid.
Mrs Berry praised the politician for facing the conference, but added: "I am sure... you felt like reaching for a stab-proof vest and perhaps slipping into old habits and lighting up to calm your nerves.
"But, as you have reassured us, you have moved on from these past indiscretions."
The long-running row over pay peaked in January as an estimated 22,000 officers marched on Westminster after the decision to introduce a 2.5 per cent pay rise in stages, effectively reducing the overall award to 1.9 per cent.
One delegate shouted at the Home Secretary: "Give us our money."
Mrs Berry went on: "Your decision not to honour the pay award was a breach of faith.
"It was a monumental mistake, and I don't say this lightly when I say you betrayed the police service.
"How was it that the Government found £2.7bn to dig itself out of a tax hole in advance of a by-election but couldn't find £30m to honour our pay deal?"
The Home Secretary's appearance in Bournemouth came the day after officers voted to lobby for the same rights as other workers, including the right to strike.
Ms Smith responded with a series of improvements to police remuneration and announcements on funding and policy.
During the conference session, she appeared to agree to abide by the result of a High Court judicial review of her decision not to award the full pay award - a ruling which is due to be announced within days.
But she later left open the possibility of a Home Office appeal if the decision goes against her.
"We will follow what the judicial system decides we should do. Where the judicial system ends up, we will honour that," she said.
Speaking about the pay row, Ms Smith said she stood by her decision despite the anger it caused.
She told delegates: "I know you strongly disagree with the decision. But it was one that I took only after a lot of thought - after considering the full facts of the case, the need to keep mortgages and the cost of living under control - and that includes your mortgages and your families' cost of living as well.
"There was another crucial factor at play - affordability, and for that read police officer numbers.
"I needed to ensure that you continued to have your colleagues working alongside you. All your colleagues.
"At a time when families are feeling the pinch, I know how important it is to restore stability and confidence into discussions on your pay."
Ms Smith said any long-term deal agreed on an index created by the arbitration tribunal would be fully implemented.
She added: "But let's be under no illusions. Setting out on the road to strike will lead only to a dead end."
Ms Smith told delegates that retirement lump sum payments would be recalculated at a cost of £100m to the Treasury, significantly increasing the amount for many officers.
And she said partners of those killed in service should continue to receive their full pension regardless of whether they remarry.
Ms Smith also said an oversubscribed £50m fund for handheld computers would be extended.
She said that if trials of electric stun guns showed they protected police and the public they would be "issued routinely" to all officers.
The Government would scrap stop and account forms, reduce data it collected by a third, and simplify custody, bail and premises entry procedures, she added.
Ms Smith also announced that a "senior figure" would be appointed to oversee how Government policy changes impacted on frontline officers.
Yesterday's vote was a step towards the first police strike for nearly 90 years.
The police last went on strike in 1918 and 1919 in Liverpool and London, leading to the Government banning officers from taking industrial action or belonging to a trade union.
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