diff --git a/build/ci/stage-build-linux-tests.yml b/build/ci/stage-build-linux-tests.yml
index 4d6e2d294..31dc984d1 100644
--- a/build/ci/stage-build-linux-tests.yml
+++ b/build/ci/stage-build-linux-tests.yml
@@ -45,6 +45,12 @@ jobs:
       OverWrite: false
       flattenFolders: false
 
+  ## Validate dotnet.js fingerprint matches actual file
+  - bash: |
+      $(build.sourcesdirectory)/build/scripts/validate-dotnetjs-fingerprint.sh \
+        "$(build.sourcesdirectory)/src/Uno.Wasm.Sample.RayTracer/bin/Release/net10.0/publish/wwwroot"
+    displayName: Validate dotnet.js fingerprint (RayTracer)
+
   ## Raytracer validation
   - bash: |
       $(build.sourcesdirectory)/build/scripts/run-tests.sh \
@@ -102,6 +108,12 @@ jobs:
       OverWrite: false
       flattenFolders: false
 
+  ## Validate dotnet.js fingerprint matches actual file (SWA build)
+  - bash: |
+      $(build.sourcesdirectory)/build/scripts/validate-dotnetjs-fingerprint.sh \
+        "$(build.sourcesdirectory)/src/Uno.Wasm.Sample.RayTracer/bin/Release/net10.0/publish/wwwroot"
+    displayName: Validate dotnet.js fingerprint (SWA)
+
   - bash: |
       $(build.sourcesdirectory)/build/scripts/run-tests-swa.sh \
         "$(build.sourcesdirectory)/src/Uno.Wasm.Sample.RayTracer/bin/Release/net10.0/publish/wwwroot" \
diff --git a/build/ci/stage-build-macos-tests.yml b/build/ci/stage-build-macos-tests.yml
index 01add7a86..5082fbc99 100644
--- a/build/ci/stage-build-macos-tests.yml
+++ b/build/ci/stage-build-macos-tests.yml
@@ -33,6 +33,12 @@ jobs:
       dotnet publish -c Release /m:1 /p:DISABLE_CLIHOST_NET6=true /p:WasmShellEmccLinkOptimization=false /p:WasmShellILLinkerEnabled=false /bl:$(build.artifactstagingdirectory)/SampleNet5-nolinker-macos.binlog
     displayName: Build StaticLinking.Interpreter Sample (net5 without linker)
 
+  ## Validate dotnet.js fingerprint matches actual file
+  - bash: |
+      $(build.sourcesdirectory)/build/scripts/validate-dotnetjs-fingerprint.sh \
+        "$(build.sourcesdirectory)/src/Uno.Wasm.StaticLinking.Interpreter/bin/Release/net10.0/publish/wwwroot"
+    displayName: Validate dotnet.js fingerprint (StaticLinking.Interpreter)
+
   - bash: |
       $(build.sourcesdirectory)/build/scripts/run-tests.sh \
         "$(build.sourcesdirectory)/src/Uno.Wasm.StaticLinking.Interpreter/bin/Release/net10.0/publish/wwwroot" \
diff --git a/build/ci/stage-build-windows-tests.yml b/build/ci/stage-build-windows-tests.yml
index 6c2e409a8..50cdf0860 100644
--- a/build/ci/stage-build-windows-tests.yml
+++ b/build/ci/stage-build-windows-tests.yml
@@ -66,10 +66,16 @@ jobs:
 
   - pwsh: |
       cd $(build.sourcesdirectory)/src/Uno.Wasm.Sample.RayTracer
-      dotnet clean -c Release 
+      dotnet clean -c Release
       dotnet publish -c Release /m:1  /p:WasmShellEmccLinkOptimization=false /bl:$(build.artifactstagingdirectory)/SampleNet5-win.binlog
     displayName: Build Raytracer Sample
 
+  ## Validate dotnet.js fingerprint matches actual file
+  - pwsh: |
+      $(build.sourcesdirectory)\build\scripts\validate-dotnetjs-fingerprint.ps1 `
+        -PublishPath "$(build.sourcesdirectory)\src\Uno.Wasm.Sample.RayTracer\bin\Release\net10.0\publish\wwwroot"
+    displayName: Validate dotnet.js fingerprint (RayTracer)
+
   - pwsh: |
       $(build.sourcesdirectory)\build\scripts\run-tests-windows.ps1 `
       "$(build.sourcesdirectory)\src\Uno.Wasm.Sample.RayTracer\bin\Release\net10.0\publish\wwwroot" `
diff --git a/build/scripts/validate-dotnetjs-fingerprint.ps1 b/build/scripts/validate-dotnetjs-fingerprint.ps1
new file mode 100644
index 000000000..40b1a68e3
--- /dev/null
+++ b/build/scripts/validate-dotnetjs-fingerprint.ps1
@@ -0,0 +1,50 @@
+# Validates that uno-config.js references a dotnet.js fingerprint that matches an actual file
+param(
+    [Parameter(Mandatory=$true)]
+    [string]$PublishPath
+)
+
+$ErrorActionPreference = "Stop"
+
+Write-Host "Validating dotnet.js fingerprint in: $PublishPath"
+
+# Find uno-config.js (it could be in a package_* subdirectory)
+$unoConfig = Get-ChildItem -Path $PublishPath -Recurse -Filter "uno-config.js" | Select-Object -First 1
+
+if (-not $unoConfig) {
+    Write-Host "ERROR: uno-config.js not found in $PublishPath"
+    exit 1
+}
+
+Write-Host "Found uno-config.js: $($unoConfig.FullName)"
+
+# Read the content and extract the fingerprint
+$content = Get-Content -Path $unoConfig.FullName -Raw
+$match = [regex]::Match($content, 'dotnet\.([a-z0-9]+)\.js')
+
+if (-not $match.Success) {
+    Write-Host "ERROR: Could not extract dotnet.js fingerprint from uno-config.js"
+    Write-Host "Content of uno-config.js:"
+    Write-Host $content
+    exit 1
+}
+
+$fingerprint = $match.Groups[1].Value
+Write-Host "Fingerprint in uno-config.js: $fingerprint"
+
+# Check if the fingerprinted dotnet.js file exists
+$frameworkPath = Join-Path $PublishPath "_framework"
+$dotnetJsFile = Join-Path $frameworkPath "dotnet.$fingerprint.js"
+
+if (-not (Test-Path $dotnetJsFile)) {
+    Write-Host "ERROR: Fingerprint mismatch!"
+    Write-Host "  uno-config.js references: dotnet.$fingerprint.js"
+    Write-Host "  But this file does not exist in: $frameworkPath"
+    Write-Host ""
+    Write-Host "Available dotnet.*.js files in _framework:"
+    Get-ChildItem -Path $frameworkPath -Filter "dotnet.*.js" -ErrorAction SilentlyContinue | ForEach-Object { Write-Host "  $($_.Name)" }
+    exit 1
+}
+
+Write-Host "SUCCESS: dotnet.$fingerprint.js exists in _framework"
+Write-Host "Fingerprint validation passed!"
diff --git a/build/scripts/validate-dotnetjs-fingerprint.sh b/build/scripts/validate-dotnetjs-fingerprint.sh
new file mode 100755
index 000000000..0a1bd8f7a
--- /dev/null
+++ b/build/scripts/validate-dotnetjs-fingerprint.sh
@@ -0,0 +1,51 @@
+#!/bin/bash
+# Validates that uno-config.js references a dotnet.js fingerprint that matches an actual file
+set -e
+
+PUBLISH_PATH=$1
+
+if [ -z "$PUBLISH_PATH" ]; then
+    echo "Usage: validate-dotnetjs-fingerprint.sh <publish-wwwroot-path>"
+    exit 1
+fi
+
+echo "Validating dotnet.js fingerprint in: $PUBLISH_PATH"
+
+# Find uno-config.js (it could be in a package_* subdirectory)
+UNO_CONFIG=$(find "$PUBLISH_PATH" -name "uno-config.js" -type f | head -1)
+
+if [ -z "$UNO_CONFIG" ]; then
+    echo "ERROR: uno-config.js not found in $PUBLISH_PATH"
+    exit 1
+fi
+
+echo "Found uno-config.js: $UNO_CONFIG"
+
+# Extract the fingerprint from uno-config.js (portable across GNU and BSD grep/sed)
+FINGERPRINT=$(sed -n 's/.*dotnet\.\([a-z0-9]*\)\.js.*/\1/p' "$UNO_CONFIG" | head -1)
+
+if [ -z "$FINGERPRINT" ]; then
+    echo "ERROR: Could not extract dotnet.js fingerprint from uno-config.js"
+    echo "Content of uno-config.js:"
+    cat "$UNO_CONFIG"
+    exit 1
+fi
+
+echo "Fingerprint in uno-config.js: $FINGERPRINT"
+
+# Check if the fingerprinted dotnet.js file exists
+FRAMEWORK_PATH="$PUBLISH_PATH/_framework"
+DOTNET_JS_FILE="$FRAMEWORK_PATH/dotnet.$FINGERPRINT.js"
+
+if [ ! -f "$DOTNET_JS_FILE" ]; then
+    echo "ERROR: Fingerprint mismatch!"
+    echo "  uno-config.js references: dotnet.$FINGERPRINT.js"
+    echo "  But this file does not exist in: $FRAMEWORK_PATH"
+    echo ""
+    echo "Available dotnet.*.js files in _framework:"
+    ls -la "$FRAMEWORK_PATH"/dotnet.*.js 2>/dev/null || echo "  (none found)"
+    exit 1
+fi
+
+echo "SUCCESS: dotnet.$FINGERPRINT.js exists in _framework"
+echo "Fingerprint validation passed!"
diff --git a/src/Uno.Wasm.Bootstrap/build/Uno.Wasm.Bootstrap.targets b/src/Uno.Wasm.Bootstrap/build/Uno.Wasm.Bootstrap.targets
index 4c6d40bd4..172bc9088 100644
--- a/src/Uno.Wasm.Bootstrap/build/Uno.Wasm.Bootstrap.targets
+++ b/src/Uno.Wasm.Bootstrap/build/Uno.Wasm.Bootstrap.targets
@@ -452,15 +452,18 @@
 			AfterTargets="ResolvePublishStaticWebAssets">
 
 		<!-- Find the dotnet.js StaticWebAsset from publish assets and extract its fingerprint.
-		     We look for assets where AssetMode is 'All' or 'Publish' to get the publish-time fingerprint. -->
+		     We look for assets where AssetMode is 'All' or 'Publish' to get the publish-time fingerprint.
+		     During publish, the RelativePath may already be resolved to the actual fingerprinted value
+		     (e.g., '_framework/dotnet.abc123.js') instead of the placeholder pattern, so we match both. -->
 		<ItemGroup>
 			<_UnoDotnetJsAssetPublish Include="@(StaticWebAsset)"
-				Condition="$([System.String]::Copy('%(RelativePath)').StartsWith('_framework/dotnet#[.{fingerprint}]')) AND $([System.String]::Copy('%(RelativePath)').EndsWith('.js')) AND !$([System.String]::Copy('%(RelativePath)').Contains('.native')) AND !$([System.String]::Copy('%(RelativePath)').Contains('.runtime')) AND ('%(AssetMode)' == 'All' OR '%(AssetMode)' == 'Publish' OR '%(AssetMode)' == '')" />
+				Condition="($([System.String]::Copy('%(RelativePath)').StartsWith('_framework/dotnet#[.{fingerprint}]')) OR $([System.Text.RegularExpressions.Regex]::IsMatch('%(RelativePath)', '^_framework/dotnet\.[a-z0-9]+\.js$'))) AND $([System.String]::Copy('%(RelativePath)').EndsWith('.js')) AND !$([System.String]::Copy('%(RelativePath)').Contains('.native')) AND !$([System.String]::Copy('%(RelativePath)').Contains('.runtime')) AND ('%(AssetMode)' == 'All' OR '%(AssetMode)' == 'Publish' OR '%(AssetMode)' == '')" />
 		</ItemGroup>
 
-		<!-- Get the last fingerprint (which should be the publish one) by using batching -->
+		<!-- Get the fingerprint from metadata first, then fall back to extracting from RelativePath if empty -->
 		<PropertyGroup>
 			<_UnoDotnetJsFingerprintPublish>%(_UnoDotnetJsAssetPublish.Fingerprint)</_UnoDotnetJsFingerprintPublish>
+			<_UnoDotnetJsFingerprintPublish Condition="'$(_UnoDotnetJsFingerprintPublish)' == ''">$([System.Text.RegularExpressions.Regex]::Match('%(_UnoDotnetJsAssetPublish.RelativePath)', 'dotnet\.([a-z0-9]+)\.js$').Groups[1].Value)</_UnoDotnetJsFingerprintPublish>
 			<_UnoConfigJsPath>$(IntermediateOutputPath)unowwwrootassets/uno-config.js</_UnoConfigJsPath>
 		</PropertyGroup>
 
diff --git a/src/Uno.Wasm.Sample.RayTracer/Uno.Wasm.Sample.RayTracer.csproj b/src/Uno.Wasm.Sample.RayTracer/Uno.Wasm.Sample.RayTracer.csproj
index 9c2049663..b32a8c2a6 100644
--- a/src/Uno.Wasm.Sample.RayTracer/Uno.Wasm.Sample.RayTracer.csproj
+++ b/src/Uno.Wasm.Sample.RayTracer/Uno.Wasm.Sample.RayTracer.csproj
@@ -56,6 +56,9 @@
 		<PropertyGroup>
 			<_appOutput>$(PublishDir)wwwroot/$(WasmShellOutputPackagePath)</_appOutput>
 			<_unoConfigJsContent>$([System.IO.File]::ReadAllText('$(_appOutput)/uno-config.js'))</_unoConfigJsContent>
+			<_frameworkPath>$(PublishDir)wwwroot/_framework</_frameworkPath>
+			<!-- Extract the fingerprint from uno-config.js to verify the file exists -->
+			<_configDotnetJsFingerprint>$([System.Text.RegularExpressions.Regex]::Match('$(_unoConfigJsContent)', 'dotnet\.([a-z0-9]+)\.js').Groups[1].Value)</_configDotnetJsFingerprint>
 		</PropertyGroup>
 
 		<ItemGroup>
@@ -72,6 +75,10 @@
 		<Error Condition="$(_unoConfigJsContent.Contains('_framework/dotnet.js'))"
 			   Text="uno-config.js contains non-fingerprinted _framework/dotnet.js reference in offline_files. Expected fingerprinted path like '_framework/dotnet.abc123.js'" />
 
+		<!-- Validate that the fingerprinted dotnet.js file referenced in uno-config.js actually exists -->
+		<Error Condition="'$(_configDotnetJsFingerprint)' != '' AND !Exists('$(_frameworkPath)/dotnet.$(_configDotnetJsFingerprint).js')"
+			   Text="Fingerprint mismatch: uno-config.js references dotnet.$(_configDotnetJsFingerprint).js but this file does not exist in $(_frameworkPath). The publish-time fingerprint update may have failed." />
+
 		<Message Importance="high" Text="Output dist validated" />
 	</Target>