diff --git a/CHANGELOG.md b/CHANGELOG.md
index aae74ac26..f13c44044 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -21,6 +21,7 @@ The following emojis are used to highlight certain changes:
 
 ### Changed
 
+- 🛠 `files`: `File` interface no longer embeds `io.Seeker`. Implementations that support seeking (e.g. `ReaderFile` wrapping a seekable reader, `Symlink`, UnixFS files) still have a `Seek` method, but callers must type-assert to `io.Seeker` instead of assuming all files are seekable. This fixes interface-sniffing bugs where non-seekable readers (HTTP multipart streams, `WebFile`) falsely advertised seek support and caused runtime errors in downstream consumers like `go-car`. [#1128](https://github.com/ipfs/boxo/pull/1128)
 - `chunker`: `FromString` now rejects malformed `size-` strings with extra parameters (e.g. `size-123-extra` was previously silently accepted).
 - upgrade to `go-libp2p` [v0.48.0](https://github.com/libp2p/go-libp2p/releases/tag/v0.48.0)
 
diff --git a/files/doc.go b/files/doc.go
index 69c7dc550..6d6f2a9ba 100644
--- a/files/doc.go
+++ b/files/doc.go
@@ -6,7 +6,7 @@
 // The package defines a hierarchy of interfaces:
 //
 //   - [Node]: Base interface for all file-like objects (mode, modification time, size)
-//   - [File]: A regular file with [io.Reader] and [io.Seeker]
+//   - [File]: A regular file with [io.Reader] (some implementations also support [io.Seeker])
 //   - [Directory]: Contains entries traversable via [DirIterator]
 //   - [FileInfo]: Extends [Node] with local filesystem information
 //
diff --git a/files/file.go b/files/file.go
index e2ece2862..f9feda660 100644
--- a/files/file.go
+++ b/files/file.go
@@ -32,12 +32,16 @@ type Node interface {
 	Size() (int64, error)
 }
 
-// Node represents a regular Unix file
+// File represents a regular Unix file.
+//
+// Implementations that support random access may also implement [io.Seeker].
+// Callers that need seeking should type-assert rather than assume all Files
+// are seekable, since some implementations (e.g. HTTP multipart streams)
+// only support sequential reads.
 type File interface {
 	Node
 
 	io.Reader
-	io.Seeker
 }
 
 // DirEntry exposes information about a directory entry
diff --git a/files/webfile.go b/files/webfile.go
index 6cc9d5782..b64672f08 100644
--- a/files/webfile.go
+++ b/files/webfile.go
@@ -100,11 +100,6 @@ func (wf *WebFile) Close() error {
 	return wf.body.Close()
 }
 
-// TODO: implement
-func (wf *WebFile) Seek(offset int64, whence int) (int64, error) {
-	return 0, ErrNotSupported
-}
-
 func (wf *WebFile) Size() (int64, error) {
 	if err := wf.start(); err != nil {
 		return 0, err
diff --git a/gateway/backend_blocks.go b/gateway/backend_blocks.go
index 45b11c327..59590978f 100644
--- a/gateway/backend_blocks.go
+++ b/gateway/backend_blocks.go
@@ -175,7 +175,11 @@ func (bb *BlocksBackend) Get(ctx context.Context, path path.ImmutablePath, range
 		}
 
 		if rootCodec == uint64(mc.Raw) {
-			if err := seekToRangeStart(f, ra, fileSize); err != nil {
+			s, ok := f.(io.Seeker)
+			if !ok {
+				return ContentPathMetadata{}, nil, fmt.Errorf("file does not support seeking: %w", ErrInternalServerError)
+			}
+			if err := seekToRangeStart(s, ra, fileSize); err != nil {
 				return ContentPathMetadata{}, nil, err
 			}
 		}
@@ -216,8 +220,12 @@ func (bb *BlocksBackend) Get(ctx context.Context, path path.ImmutablePath, range
 			return ContentPathMetadata{}, nil, err
 		}
 
-		if err := seekToRangeStart(file, ra, fileSize); err != nil {
-			return ContentPathMetadata{}, nil, err
+		if seeker, ok := file.(io.Seeker); ok {
+			if err := seekToRangeStart(seeker, ra, fileSize); err != nil {
+				return ContentPathMetadata{}, nil, err
+			}
+		} else if ra != nil && ra.From != 0 {
+			return ContentPathMetadata{}, nil, fmt.Errorf("file does not support seeking: %w", ErrInternalServerError)
 		}
 
 		if s, ok := f.(*files.Symlink); ok {
@@ -279,7 +287,12 @@ func loadUnixFSFileWithLazyBlocks(ctx context.Context, path path.ImmutablePath,
 	}
 
 	// Seek to the start of the requested range
-	if err := seekToRangeStart(file, ra, fileSize); err != nil {
+	seeker, ok := file.(io.Seeker)
+	if !ok {
+		log.Debugw("file does not support seeking, skipping range optimization", "path", path)
+		return nil
+	}
+	if err := seekToRangeStart(seeker, ra, fileSize); err != nil {
 		log.Debugw("failed to seek to range start",
 			"path", path,
 			"error", err)
diff --git a/gateway/backend_car.go b/gateway/backend_car.go
index aaa20258a..f89616c64 100644
--- a/gateway/backend_car.go
+++ b/gateway/backend_car.go
@@ -470,7 +470,11 @@ func loadTerminalEntity(ctx context.Context, c cid.Cid, blk blocks.Block, lsys *
 					return nil, fmt.Errorf("invalid car backend range: negative start bigger than the file size")
 				}
 			}
-			if _, err := f.Seek(from, io.SeekStart); err != nil {
+			s, ok := f.(io.Seeker)
+			if !ok {
+				return nil, fmt.Errorf("file does not support seeking")
+			}
+			if _, err := s.Seek(from, io.SeekStart); err != nil {
 				return nil, err
 			}
 		}
diff --git a/gateway/backend_car_files.go b/gateway/backend_car_files.go
index 8bae0ebcf..14522aa67 100644
--- a/gateway/backend_car_files.go
+++ b/gateway/backend_car_files.go
@@ -102,9 +102,9 @@ func (b *backpressuredFile) Read(p []byte) (n int, err error) {
 			continue
 		}
 
-		f, ok := nd.(files.File)
+		f, ok := nd.(io.ReadSeeker)
 		if !ok {
-			return 0, fmt.Errorf("not a file, should be unreachable")
+			return 0, fmt.Errorf("not a seekable file, should be unreachable")
 		}
 
 		b.f = f
diff --git a/gateway/backend_car_test.go b/gateway/backend_car_test.go
index 029b96c71..29d8a7368 100644
--- a/gateway/backend_car_test.go
+++ b/gateway/backend_car_test.go
@@ -604,7 +604,8 @@ func TestCarBackendGetFileRangeRequest(t *testing.T) {
 	uio, err := unixfile.NewUnixfsFile(ctx, dsrv, fileRootNd)
 	require.NoError(t, err)
 	f := uio.(files.File)
-	_, err = f.Seek(int64(startIndex), io.SeekStart)
+	fSeeker := f.(io.Seeker)
+	_, err = fSeeker.Seek(int64(startIndex), io.SeekStart)
 	require.NoError(t, err)
 	expectedFileData, err := io.ReadAll(io.LimitReader(f, int64(endIndex)-int64(startIndex)+1))
 	require.NoError(t, err)
diff --git a/gateway/handler_block.go b/gateway/handler_block.go
index 27507272e..d5825d84e 100644
--- a/gateway/handler_block.go
+++ b/gateway/handler_block.go
@@ -2,6 +2,8 @@ package gateway
 
 import (
 	"context"
+	"fmt"
+	"io"
 	"net/http"
 	"time"
 
@@ -44,7 +46,12 @@ func (i *handler) serveRawBlock(ctx context.Context, w http.ResponseWriter, r *h
 		return false
 	}
 
-	if !i.seekToStartOfFirstRange(w, r, data, sz) {
+	s, ok := data.(io.Seeker)
+	if !ok {
+		i.webError(w, r, fmt.Errorf("block data does not support seeking"), http.StatusInternalServerError)
+		return false
+	}
+	if !i.seekToStartOfFirstRange(w, r, s, sz) {
 		return false
 	}
 
diff --git a/gateway/handler_codec.go b/gateway/handler_codec.go
index 414c89900..6569bb6d2 100644
--- a/gateway/handler_codec.go
+++ b/gateway/handler_codec.go
@@ -78,7 +78,12 @@ func (i *handler) serveCodec(ctx context.Context, w http.ResponseWriter, r *http
 		return false
 	}
 
-	return i.renderCodec(ctx, w, r, rq, blockSize, data)
+	rsc, ok := data.(io.ReadSeekCloser)
+	if !ok {
+		i.webError(w, r, fmt.Errorf("block data does not support seeking"), http.StatusInternalServerError)
+		return false
+	}
+	return i.renderCodec(ctx, w, r, rq, blockSize, rsc)
 }
 
 func (i *handler) renderCodec(ctx context.Context, w http.ResponseWriter, r *http.Request, rq *requestData, blockSize int64, blockData io.ReadSeekCloser) bool {