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Destin, FL Office Buildings for Sale

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Miramar Beach, FL Shalimar, FL Fort Walton Beach, FL Freeport, FL Niceville, FL Valparaiso, FL Mary Esther, FL Santa Rosa Beach, FL
Class A Office Building with Balconies
Updated: Apr 10
Class A Office Building with Balconies

4481 Legendary Dr, Destin, FL 32541

Contact for pricing
9,672 sqft
3‑story Class A office building in the Regatta Bay Office Park
9,672 SF of heated and cooled space
Additional 1,820 SF of balcony/veranda space overlooking the Regatta Bay entry lake
Part of a 120‑acre PUD with 28 acres of lakes and pristine common areas
Linked to the Destin Commons Shopping District for year‑round entertainment and shopping
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Freestanding Office Buildings with Marquis
Updated: Nov 10, 2025
Freestanding Office Buildings with Marquis

36250 Emerald Coast Parkway Unit 250 & 25, Destin, FL 32541

Contact for pricing
3,567 sqft
Two freestanding office buildings on a hard corner at a signalized intersection on Emerald Coast Parkway and Trista Terrace Court in Destin, FL
HD‑quality electronic marquis sign with visibility to traffic counts up to 54,000 AADT per day
Hard corner building (Bldg 250): 3,567 SF with 7 offices, 2 bkrs, ADA bathrooms, elevator, and conference room
Bldg 250 includes large 3rd‑floor H/C storage room and 14 parking spaces
Second building (Bldg 254): 3,776 SF with lobby and reception, 6 offices, break room, and conference room
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Office
Office

34990 Emerald Coast Parkway, Destin, FL 32541

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24,170 sqft

Office buildings · 24,170 SF

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Turn a Listing Into an Investment Snapshot Cap Rate, Potential NOI, Demand score for every listing. Go To Analytics Center
Based on your search, we've compiled 62 Potential Opportunities for your consideration. Besides 3 Active listings in Destin, FL, we suggest exploring several alternatives: 4 properties in Nearby Cities, and similar 54 Off-Market properties to explore as potential leads, plus 1 Land Listings that present a potential for development.

Opportunities in Nearby Cities

Here are 4 Similar properties we found in Nearby Locations for your consideration.

Fort Walton Beach Office Building
Fort Walton Beach Office Building

30 Ferry Rd SE, Fort Walton Beach, FL 32548

$670,000
2,208 sqft

NNN leased office building in Fort Walton Beach, Florida.

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Freestanding Medical Office Building
Freestanding Medical Office Building

28 Perry Ave SE, Fort Walton Beach, FL 32548

Contact for pricing
3,432 sqft

Single-story healthcare facility with reception, exam, restroom, kitchen, and light manufacturing areas.

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Class A Office Administration Building
Class A Office Administration Building

511 Government Avenue Unit 300, Valparaiso, FL 32580

Contact for pricing
123,500 sqft

State-of-the-art Class A office building with dining and a community room accommodating up to 300 people.

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Class A Office Building
Class A Office Building

511 Government Avenue Unit 200, Valparaiso, FL 32580

Contact for pricing
123,500 sqft

New Class A office building with public dining, green space, and a community room.

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Potential Development Sites for Consideration

Can't find the perfect fit? These Land listings present an alternative path: the potential to develop a property for your specific goals.

Important: These AI-suggestions are a starting point, not a guarantee of permitted use. All zoning, permitting, and land use information must be independently verified by you with the appropriate local authorities before making any commitments.

Coastal Center Commercial Land
Coastal Center Commercial Land

1939 Mack Bayou Road, Santa Rosa Beach, FL 32459

$4,995,000
13.02 AC lot

Commercial land with Coastal Center zoning adjacent to a golf course.

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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
OFFICE BUILDING

1209 Airport Rd Ste, Destin, FL 32541-2933

Unit 3
Value Estimation by Request
1,000 sqft 0.02 AC lot
View details
1209 Airport Rd Ste, Unit 1
OFFICE BUILDING

1209 Airport Rd Ste, Destin, FL 32541-2933

Unit 1
$495,000
Estimated value
3,000 sqft 0.07 AC lot
View details
1209 Airport Rd Ste, Unit 2
OFFICE BUILDING

1209 Airport Rd Ste, Destin, FL 32541-2933

Unit 2
$185,000
Estimated value
1,000 sqft 0.02 AC lot
View details
415 Mtn Dr Ste, Unit 9
OFFICE BUILDING

415 Mtn Dr Ste, Destin, FL 32541-7310

Unit 9
$210,000
Estimated value
972 sqft 0.02 AC lot
View details
160th Industrial Park Rd
OFFICE BUILDING

160th Industrial Park Rd, Destin, FL 32541-2707

$1,500,000
Estimated value
View details
415 Mtn Dr Ste, Unit 1
OFFICE BUILDING

415 Mtn Dr Ste, Destin, FL 32541-2349

Unit 1
$295,000
Estimated value
1,779 sqft 0.02 AC lot
View details
415 Mtn Dr Ste, Unit 3
OFFICE BUILDING

415 Mtn Dr Ste, Destin, FL 32541-2349

Unit 3
$345,000
Estimated value
1,809 sqft 0.04 AC lot
View details
625 Hbr Blvd
OFFICE BUILDING

625 Hbr Blvd, Destin, FL 32541-2465

$235,000
Estimated value
996 sqft 0.02 AC lot
View details
4510 Turnberry Harbour Dr
OFFICE BUILDING

4510 Turnberry Harbour Dr, Destin, FL 32541-6301

$2,165,000
Estimated value
13.55 AC lot
View details
557 Mack Byu Rd
OFFICE BUILDING

557 Mack Byu Rd, Destin, FL 32550

$145,000
Estimated value
1,024 sqft 0.46 AC lot
View details
415 Mtn Dr Ste, Unit 5
OFFICE BUILDING

415 Mtn Dr Ste, Destin, FL 32541-2349

Unit 5
$215,000
Estimated value
2,208 sqft 0.04 AC lot
View details
600 Hbr Blvd
OFFICE BUILDING

600 Hbr Blvd, Destin, FL 32541-2426

$2,685,000
Estimated value
3,172 sqft 0.18 AC lot
View details
585 Mack Byu Rd
OFFICE BUILDING

585 Mack Byu Rd, Destin, FL 32550

$535,000
Estimated value
4,064 sqft 0.36 AC lot
View details
1209 Airport Rd Ste, Unit 5
OFFICE BUILDING

1209 Airport Rd Ste, Destin, FL 32541-2933

Unit 5
$205,000
Estimated value
1,000 sqft 0.02 AC lot
View details
215 Mtn Dr Ste, Unit 112
OFFICE BUILDING

215 Mtn Dr Ste, Destin, FL 32541-2346

Unit 112
$245,000
Estimated value
1,130 sqft 0.03 AC lot
View details
215 Mtn Dr Ste, Unit 111
OFFICE BUILDING

215 Mtn Dr Ste, Destin, FL 32541-2346

Unit 111
$240,000
Estimated value
1,130 sqft 0.03 AC lot
View details
215 Mtn Dr Ste, Unit 110
OFFICE BUILDING

215 Mtn Dr Ste, Destin, FL 32541-2346

Unit 110
$235,000
Estimated value
1,130 sqft 0.03 AC lot
View details
215 Mtn Dr Ste, Unit 109
OFFICE BUILDING

215 Mtn Dr Ste, Destin, FL 32541-2346

Unit 109
$240,000
Estimated value
1,130 sqft 0.03 AC lot
View details
215 Mtn Dr Ste, Unit 108
OFFICE BUILDING

215 Mtn Dr Ste, Destin, FL 32541-2346

Unit 108
$240,000
Estimated value
1,130 sqft 0.03 AC lot
View details
215 Mtn Dr Ste, Unit 107
OFFICE BUILDING

215 Mtn Dr Ste, Destin, FL 32541-2346

Unit 107
$275,000
Estimated value
1,496 sqft 0.03 AC lot
View details
215 Mtn Dr Ste, Unit 106
OFFICE BUILDING

215 Mtn Dr Ste, Destin, FL 32541-2346

Unit 106
$275,000
Estimated value
1,496 sqft 0.03 AC lot
View details

Destin, FL Office Buildings Market Trends and Statistics

Explore 57 office buildings for sale in Destin, FL, showcased through 3 active listings on our real estate platform. These investment opportunities span a total of 37,409 square feet of properties for sale.

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Top Commercial Asset Segments

Commercial property segments ranked by active listings on the market

Office Units 76
Office buildings 19
Medical Office Space 5
Coworking space 4

Demographics Overview

Population 27K
Population Growth (5Y) -2.5%
Median Household Income $94,001
College Educated 46.2%

High-Yield Neighborhoods for Investment

Identify Destin submarkets with the highest inventory density on the market and evaluate the average listing prices of real estate assets

Neighborhood Average Price
32541 $4.2M

Taxes & Financing

Tax Rate (average for all types) 1.08%
Property Tax per SF $12.52 per SF
Tax Rate vs County Average 0.16 pp below county avg
Average Loan-to-Value 65.0%

Listings Trend

New vs delisted commercial listings in Okaloosa County

New Delisted

Total CRE Inventory on Market (SF)

Average Property Price per SF

For-sale pricing trends across core commercial property types in Okaloosa County

Residential Income

Property Size Breakdown

The majority of commercial real estate listings in Destin fall within the 10,000 to 25,000 square foot range.

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