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    Destin, FL Office Buildings for Sale

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    Lehigh Acres, FL Cape Coral, FL Port Charlotte, FL
    9 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
    View details
    Harbor Blvd Commercial Office Buildings
    $1,100,000
    5,258 SF

    Harbor Blvd Commercial Office Buildings

    725 Harbor Blvd, Destin, FL

    Two office buildings on 0.46 acres with parking.

    • Highly desirable commercial location on Harbor Blvd, Destin, Florida.
    • Two office buildings on a .46 acre lot.
    • Building 725 has two floors (approx. 3202 SF) and Building 727 is a single level (approx. 2056 SF).
    • Front and rear parking available.
    • Convenient driveway access opening to Harbor Blvd.
    Updated: Nov 25, 2025
    View details
    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
    View details
    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
    View details
    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
    View details
    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
    View details
    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
    View details
    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
    View details
    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
    View details
    Based on your search, we've compiled 71 Potential Opportunities for your consideration. Besides 9 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 4 Land Listings that present a potential for development.

    Explore Opportunities in Nearby Cities

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

    Modern Office Building For Sale
    $4,300,000

    Modern Office Building For Sale

    18,029 SF office building in prime Gulf Coast location.

    13331 Emerald Coast Parkway, Miramar Beach, FL 32550
    View details
    Two-Story Office Building in Shalimar
    $995,000

    Two-Story Office Building in Shalimar

    Two-story office building in Shalimar, Florida, totaling 6,456 square feet.

    14 11Th Avenue, Shalimar, FL 32579
    View details
    Shalimar Commercial Investment Opportunity
    $4,300,000
    31,486 SF

    Shalimar Commercial Investment Opportunity

    Commercial complex with office and restaurant tenants in Shalimar, Florida.

    60 2nd Street, Shalimar, FL 32579
    View details
    Class A Office Building
    $4,300,000
    18,029 SF

    Class A Office Building

    Three-story office building with high visibility and accessibility.

    13331 Emerald Coast Pkwy, Miramar Beach, FL 32550
    View details

    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.

    Destin Land Investment Opportunity
    $1,775,000
    1.40 Acres

    Destin Land Investment Opportunity

    Five contiguous parcels of vacant land in Destin, Florida.

    523 Sea Hills Drive, Destin, FL 32541
    View details
    Corner Parcel in Freeport, Florida
    $550,000
    4.53 Acres

    Corner Parcel in Freeport, Florida

    4.53-acre corner parcel with development potential in Freeport, Florida.

    Hwy 331, Freeport, FL 32439
    View details
    Milton, FL Industrial Land
    $1,300,000
    18.22 Acres

    Milton, FL Industrial Land

    18.22 acres of industrial land near Avalon Blvd.

    6039 Fairlands Road, Milton, FL 32583
    View details
    Prime Commercial Site Front Beach
    $549,000
    11,805 SF

    Prime Commercial Site Front Beach

    Exceptional visibility, flexible zoning, ideal for office or medical development.

    8600 Front Beach Road, Panama City Beach, FL 32407
    View details

    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
    View details
    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
    View details
    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
    415 Mtn Dr Ste, Unit 9

    415 Mtn Dr Ste, Unit 9

    OFFICE BUILDING • 972 SF
    Value Estimation by Request
    415 Mtn Dr Ste, Destin, FL 32541-7310
    View details
    160th Industrial Park Rd

    160th Industrial Park Rd

    OFFICE BUILDING
    Value Estimation
    $1,500,000
    160th Industrial Park Rd, Destin, FL 32541-2707
    View details
    415 Mtn Dr Ste, Unit 1

    415 Mtn Dr Ste, Unit 1

    OFFICE BUILDING • 1,779 SF
    Value Estimation by Request
    415 Mtn Dr Ste, Destin, FL 32541-2349
    View details
    415 Mtn Dr Ste, Unit 3

    415 Mtn Dr Ste, Unit 3

    OFFICE BUILDING • 1,809 SF
    Value Estimation by Request
    415 Mtn Dr Ste, Destin, FL 32541-2349
    View details
    625 Hbr Blvd

    625 Hbr Blvd

    OFFICE BUILDING • 996 SF
    Value Estimation by Request
    625 Hbr Blvd, Destin, FL 32541-2465
    View details
    4510 Turnberry Harbour Dr

    4510 Turnberry Harbour Dr

    OFFICE BUILDING • 13.55 Acres
    Value Estimation
    $2,085,000
    4510 Turnberry Harbour Dr, Destin, FL 32541-6301
    View details
    557 Mack Byu Rd

    557 Mack Byu Rd

    OFFICE BUILDING • 1,024 SF
    Value Estimation by Request
    557 Mack Byu Rd, Destin, FL 32550
    View details
    415 Mtn Dr Ste, Unit 5

    415 Mtn Dr Ste, Unit 5

    OFFICE BUILDING • 2,208 SF
    Value Estimation by Request
    415 Mtn Dr Ste, Destin, FL 32541-2349
    View details
    600 Hbr Blvd

    600 Hbr Blvd

    OFFICE BUILDING • 3,172 SF
    Value Estimation
    $2,465,000
    600 Hbr Blvd, Destin, FL 32541-2426
    View details
    585 Mack Byu Rd

    585 Mack Byu Rd

    OFFICE BUILDING • 4,064 SF
    Value Estimation
    $530,000
    585 Mack Byu Rd, Destin, FL 32550
    View details
    1209 Airport Rd Ste, Unit 5

    1209 Airport Rd Ste, Unit 5

    OFFICE BUILDING • 1,000 SF
    Value Estimation by Request
    1209 Airport Rd Ste, Destin, FL 32541-2933
    View details
    215 Mtn Dr Ste, Unit 112

    215 Mtn Dr Ste, Unit 112

    OFFICE BUILDING • 1,130 SF
    Value Estimation by Request
    215 Mtn Dr Ste, Destin, FL 32541-2346
    View details

    Destin, FL Office Buildings Investment Opportunities Market Analysis

    Explore 63 office buildings for sale in Destin, FL, showcased through 9 active listings on our real estate platform. These investment opportunities span a total of 3,801,171,850 square feet of properties for sale, with an estimated market value of $17,242,500.

    Sale prices for office properties in Destin, FL start at $145,000, averaging $718,437, 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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