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Destin, FL Office Properties & Spaces for Sale

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21 results
Destin Class A Office Building
$3,500,900
15,000 SF

Destin Class A Office Building

4635 Gulfstarr Drive, Destin, FL 32541

Fully leased Class A office building in Destin, Florida.

  • 6.3% CAP Rate on a Fully Leased Class A Medical/Professional Office Building
  • Generates $347,884 Annual Income
  • Prime Corner Location with High Visibility and Easy Accessibility via Traffic Light
  • 15,000+ SF of Class A Office Space with High‑Quality Finishes
  • Located in the Heart of Destin, Less Than a Mile from Destin Commons and Whole Foods
Updated: Mar 12
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Emerald Coast Office/Retail Space
Contact for pricing
3,380 SF

Emerald Coast Office/Retail Space

36164 Emerald Coast Pkwy, Destin, FL 32541

1,086 SF office/retail space near Destin's attractions and beaches.

  • High‑traffic location on Emerald Coast Pkwy (US Hwy 98) with 53,000 AADT.
  • Located near popular tourist attractions, recreational areas, and Emerald Coast beaches.
  • +/- 1,086 SF office space suitable for office or retail use.
  • Proximity to national retailers such as Publix, Walgreens, Walmart, The Home Depot, and Lowes.
  • Located in Destin, a sought‑after city with over 4 million visitors annually.
Updated: Jan 27
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Harbor Blvd Commercial Office Buildings
$1,100,000
5,258 SF

Harbor Blvd Commercial Office Buildings

Two office buildings on 0.46 acres with parking.

725 Harbor Blvd, Destin, FL
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4,029 SF Professional Office Space located on the West End of Destin For Sale
$817,500
4,314 SF

4,029 SF Professional Office Space located on the West End of Destin For Sale

4,029 SF Professional Office Space located on the West End of Destin For Sale

150 Azalea Dr, Destin, FL 32541
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Class A Office Building
$4,995,000
22,676 SF

Class A Office Building

Exceptional Class A office building in Destin, Florida for sale.

4458 Legendary Drive, Destin, FL 32541
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East Destin Office Space
$465,000
2,300 SF

East Destin Office Space

Nicely appointed office space in a mixed-use condo.

4507 Furling Ln, Destin, FL
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1,550 SF Office Condo For Sale (Pier 98 - Second Floor Suite)
$387,500
1,550 SF

1,550 SF Office Condo For Sale (Pier 98 - Second Floor Suite)

1,550 SF Office Condo For Sale (Pier 98 - Second Floor Suite)

543 Harbor Blvd, Destin, FL 32541
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Single-Story Office Building For Sale
$850,000
0.23 Acres

Single-Story Office Building For Sale

Spacious office building with front and rear parking.

727 Harbor Boulevard, Destin, FL 32541
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Destin Office Space For Sale
$200,000

Destin Office Space For Sale

Well-maintained office space in central Destin commercial center.

4507 Furling Lane #208, Destin, FL 32541
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Professional Office Space in Destin
$289,600
880 SF

Professional Office Space in Destin

Well-maintained office space in a convenient Destin location.

1221 Airport Rd Unit 207, Destin, FL 32541
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9,350 SF Large Commercial Opportunity In Prime Location In Destin For Sale
$2,995,000
13,396 SF

9,350 SF Large Commercial Opportunity In Prime Location In Destin For Sale

9,350 SF Large Commercial Opportunity In Prime Location In Destin For Sale

35000 Emerald Coast Pkwy, Destin, FL 32541
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11,340 SF Office Building For Sale
$3,200,000
11,340 SF

11,340 SF Office Building For Sale

11,340 SF Class A Three Story Office Building For Sale

4608 Opa Locka Ln, Destin, FL 32541
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Destin Office with Warehouse Building
$1,000,000
4,060 SF

Destin Office with Warehouse Building

Office with warehouse building for sale in Destin, Florida.

185 Stahlman Ave, Destin, FL 32541
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746 SF Office For Sale (543 Harbor Boulevard Unit # 101)
$217,000
746 SF

746 SF Office For Sale (543 Harbor Boulevard Unit # 101)

746 SF Office For Sale (543 Harbor Boulevard Unit # 101)

543 Harbor Blvd, Destin, FL 32541
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Destin Office Condo For Sale
$275,000
1,312 SF

Destin Office Condo For Sale

Remodeled office condo in Destin's business corridor, leased until 2026.

1217 Airport Road 419, Destin, FL 32541
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880 SF Commercial Condo Office Space For Sale
$289,000
880 SF

880 SF Commercial Condo Office Space For Sale

880 SF Commercial Condo Office Space For Sale

1219 Airport Rd, Destin, AL 32541
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Emerald Coast Parkway Office Space
Contact for pricing
3,380 SF

Emerald Coast Parkway Office Space

Office space available on Emerald Coast Parkway in Destin, Florida.

36164 Emerald Coast Parkway, Destin, FL 32541
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Class A Office Building
$4,995,000
22,676 SF

Class A Office Building

Exceptional Class A office building in Destin, Florida for sale.

4458 Legendary Drive, Destin, FL 32541
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Destin Office or Retail Space
$279,000

Destin Office or Retail Space

Mixed-use office park with office and retail space available.

114 Palmetto Street #8, Destin, FL 32541
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First Floor Office Suite
$217,000

First Floor Office Suite

First floor office suite with lobby, break area, and offices.

543 Harbor Boulevard #Ste 101, Destin, FL 32541
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First Floor Office Suite
$217,000
746 SF

First Floor Office Suite

Office suite featuring a lobby, break area, and offices.

543 Harbor Blvd, Destin, FL
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Based on your search, we've compiled Potential Opportunities for your consideration. Besides 21 Active Listings in Destin, FL, we suggest to view alternatives - similar 60 Off-Market properties to explore as potential leads.

Explore Off-Market Properties in Destin, FL

Consider similar Off-Market properties in Destin, FL. You may contact the owners directly to inquire about their potential intentions to sell. To help you make a strong first impression, we can assist by reaching out to these owners with compelling proposals created using our AI tool.

1209 Airport Rd Ste, Unit 3

1209 Airport Rd Ste, Unit 3

OFFICE BUILDING • 1,000 SF
Value Estimation by Request
1209 Airport Rd Ste, Destin, FL 32541-2933
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1209 Airport Rd Ste, Unit 1

1209 Airport Rd Ste, Unit 1

OFFICE BUILDING • 3,000 SF
Value Estimation by Request
1209 Airport Rd Ste, Destin, FL 32541-2933
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1209 Airport Rd Ste, Unit 2

1209 Airport Rd Ste, Unit 2

OFFICE BUILDING • 1,000 SF
Value Estimation by Request
1209 Airport Rd Ste, Destin, FL 32541-2933
View details

Destin, FL Office Properties & Spaces Investment Opportunities Market Analysis

Explore 81 office properties & spaces for sale in Destin, FL, showcased through 21 active listings on our real estate platform. These investment opportunities span a total of 8,188,648,589 square feet of properties for sale, with an estimated market value of $18,407,000.

Sale prices for office spaces in Destin, FL start at $145,000, averaging $681,740, and reaching up to $3,200,000 — offering options for a variety of budgets and business needs. Daily updated analytics ensure you stay ahead with the latest data and market trends.

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