diff --git a/src/Error/Error.php b/src/Error/Error.php
index 8cbc95b67..6c317bca6 100644
--- a/src/Error/Error.php
+++ b/src/Error/Error.php
@@ -41,6 +41,8 @@ class Error extends \Exception
     private $lineno;
     private $rawMessage;
     private ?Source $source;
+    private string $phpFile;
+    private int $phpLine;
 
     /**
      * Constructor.
@@ -55,6 +57,8 @@ class Error extends \Exception
     {
         parent::__construct('', 0, $previous);
 
+        $this->phpFile = $this->getFile();
+        $this->phpLine = $this->getLine();
         $this->lineno = $lineno;
         $this->source = $source;
         $this->rawMessage = $message;
@@ -111,6 +115,8 @@ class Error extends \Exception
             $this->file = $this->source->getPath();
             if ($this->lineno > 0) {
                 $this->line = $this->lineno;
+            } else {
+                $this->line = -1;
             }
         }
 
@@ -134,6 +140,7 @@ class Error extends \Exception
     {
         // $this->source is never null here (see guess() usage in Template)
 
+        $this->lineno = 0;
         $template = null;
         $templateClass = null;
         $backtrace = debug_backtrace(\DEBUG_BACKTRACE_IGNORE_ARGS | \DEBUG_BACKTRACE_PROVIDE_OBJECT);
@@ -144,6 +151,8 @@ class Error extends \Exception
                 if ($this->source->getName() === $trace['object']->getTemplateName() && !$isEmbedContainer) {
                     $template = $trace['object'];
                     $templateClass = \get_class($trace['object']);
+
+                    break;
                 }
             }
         }
@@ -158,8 +167,7 @@ class Error extends \Exception
 
         while ($e = array_pop($exceptions)) {
             $traces = $e->getTrace();
-            array_unshift($traces, ['file' => $e->getFile(), 'line' => $e->getLine()]);
-
+            array_unshift($traces, ['file' => $e instanceof Error ? $e->phpFile : $e->getFile(), 'line' => $e instanceof Error ? $e->phpLine : $e->getLine()]);
             while ($trace = array_shift($traces)) {
                 if (!isset($trace['file']) || !isset($trace['line']) || $file != $trace['file']) {
                     continue;
diff --git a/tests/ErrorTest.php b/tests/ErrorTest.php
index b0a626940..79103445e 100644
--- a/tests/ErrorTest.php
+++ b/tests/ErrorTest.php
@@ -12,13 +12,19 @@ namespace Twig\Tests;
  */
 
 use PHPUnit\Framework\TestCase;
+use Twig\Attribute\YieldReady;
+use Twig\Compiler;
 use Twig\Environment;
 use Twig\Error\Error;
 use Twig\Error\RuntimeError;
 use Twig\Error\SyntaxError;
 use Twig\Loader\ArrayLoader;
 use Twig\Loader\FilesystemLoader;
+use Twig\Loader\LoaderInterface;
+use Twig\Node\Node;
 use Twig\Source;
+use Twig\Token;
+use Twig\TokenParser\AbstractTokenParser;
 
 class ErrorTest extends TestCase
 {
@@ -253,6 +259,116 @@ EOHTML,
         }
     }
 
+    /**
+     * @dataProvider getErrorWithoutLineAndContextData
+     */
+    public function testErrorWithoutLineAndContext(LoaderInterface $loader, bool $debug, bool $addDebugInfo, bool $exceptionWithLineAndContext, int $errorLine)
+    {
+        $twig = new Environment($loader, ['debug' => $debug, 'cache' => false]);
+        $twig->removeCache('no_line_and_context_exception.twig');
+        $twig->removeCache('no_line_and_context_exception_include_line_5.twig');
+        $twig->removeCache('no_line_and_context_exception_include_line_1.twig');
+        $twig->addTokenParser(new class($addDebugInfo, $exceptionWithLineAndContext) extends AbstractTokenParser {
+            public function __construct(private bool $addDebugInfo, private bool $exceptionWithLineAndContext)
+            {
+            }
+
+            public function parse(Token $token)
+            {
+                $stream = $this->parser->getStream();
+                $lineno = $stream->getCurrent()->getLine();
+                $stream->expect(Token::BLOCK_END_TYPE);
+
+                return new #[YieldReady]class($lineno, $this->addDebugInfo, $this->exceptionWithLineAndContext) extends Node
+                {
+                    public function __construct(int $lineno, private bool $addDebugInfo, private bool $exceptionWithLineAndContext)
+                    {
+                        parent::__construct([], [], $lineno);
+                    }
+
+                    public function compile(Compiler $compiler): void
+                    {
+                        if ($this->addDebugInfo) {
+                            $compiler->addDebugInfo($this);
+                        }
+                        if ($this->exceptionWithLineAndContext) {
+                            $compiler
+                                ->write('throw new \Twig\Error\RuntimeError("Runtime error.", ')
+                                ->repr($this->lineno)->raw(", \$this->getSourceContext()")
+                                ->raw(");\n")
+                            ;
+                        } else {
+                            $compiler->write('throw new \Twig\Error\RuntimeError("Runtime error.");');
+                        }
+                    }
+                };
+            }
+
+            public function getTag()
+            {
+                return 'foo';
+            }
+        });
+
+        try {
+            $twig->render('no_line_and_context_exception.twig', ['line' => $errorLine]);
+            $this->fail();
+        } catch (RuntimeError $e) {
+            if (1 === $errorLine && !$addDebugInfo && !$exceptionWithLineAndContext) {
+                // When the template only has the custom node that throws the error, we cannot find the line of the error
+                // as we have no debug info and no line and context in the exception
+                $this->assertSame(\sprintf('Runtime error in "no_line_and_context_exception_include_line_%d.twig".', $errorLine), $e->getMessage());
+                $this->assertSame(0, $e->getTemplateLine());
+            } else {
+                // When the template has some space before the custom node, the associated TextNode outputs some debug info at line 1
+                // that's why the line is 1 when we have no debug info and no line and context in the exception
+                $line = $addDebugInfo || $exceptionWithLineAndContext ? $errorLine : 1;
+                $this->assertSame(\sprintf('Runtime error in "no_line_and_context_exception_include_line_%d.twig" at line %d.', $errorLine, $line), $e->getMessage());
+                $this->assertSame($line, $e->getTemplateLine());
+            }
+
+            $line = $addDebugInfo || $exceptionWithLineAndContext ? $errorLine : 1;
+            if ($loader instanceof FilesystemLoader) {
+                $this->assertStringContainsString(\sprintf('errors/no_line_and_context_exception_include_line_%d.twig', $errorLine), $e->getFile());
+                $line = $addDebugInfo || $exceptionWithLineAndContext ? $errorLine : (1 === $errorLine ? -1 : 1);
+                $this->assertSame($line, $e->getLine());
+            } else {
+                $this->assertStringContainsString('Environment.php', $e->getFile());
+                $this->assertNotSame($line, $e->getLine());
+            }
+        }
+    }
+
+    public static function getErrorWithoutLineAndContextData(): iterable
+    {
+        $fileLoaders = [
+            new ArrayLoader([
+                'no_line_and_context_exception.twig' => "\n\n{{ include('no_line_and_context_exception_include_line_' ~ line ~ '.twig') }}",
+                'no_line_and_context_exception_include_line_5.twig' => "\n\n\n\n{% foo %}",
+                'no_line_and_context_exception_include_line_1.twig' => '{% foo %}',
+            ]),
+            new FilesystemLoader(__DIR__.'/Fixtures/errors'),
+        ];
+
+        foreach ($fileLoaders as $loader) {
+            foreach ([false, true] as $exceptionWithLineAndContext) {
+                foreach ([false, true] as $addDebugInfo) {
+                    foreach ([false, true] as $debug) {
+                        foreach ([5, 1] as $line) {
+                            $name = ($loader instanceof FilesystemLoader ? 'filesystem' : 'array')
+                                .($debug ? '_with_debug' : '_without_debug')
+                                .($addDebugInfo ? '_with_debug_info' : '_without_debug_info')
+                                .($exceptionWithLineAndContext ? '_with_context' : '_without_context')
+                                .('_line_'.$line)
+                            ;
+                            yield $name => [$loader, $debug, $addDebugInfo, $exceptionWithLineAndContext, $line];
+                        }
+                    }
+                }
+            }
+        }
+    }
+
     public static function getErroredTemplates()
     {
         return [
diff --git a/tests/Fixtures/errors/no_line_and_context_exception.twig b/tests/Fixtures/errors/no_line_and_context_exception.twig
new file mode 100644
index 000000000..4059c7485
--- /dev/null
+++ b/tests/Fixtures/errors/no_line_and_context_exception.twig
@@ -0,0 +1,3 @@
+
+
+{{ include('no_line_and_context_exception_include_line_' ~ line ~ '.twig') }}
diff --git a/tests/Fixtures/errors/no_line_and_context_exception_include_line_1.twig b/tests/Fixtures/errors/no_line_and_context_exception_include_line_1.twig
new file mode 100644
index 000000000..9a2e6ffa6
--- /dev/null
+++ b/tests/Fixtures/errors/no_line_and_context_exception_include_line_1.twig
@@ -0,0 +1 @@
+{% foo %}
diff --git a/tests/Fixtures/errors/no_line_and_context_exception_include_line_5.twig b/tests/Fixtures/errors/no_line_and_context_exception_include_line_5.twig
new file mode 100644
index 000000000..bb229015a
--- /dev/null
+++ b/tests/Fixtures/errors/no_line_and_context_exception_include_line_5.twig
@@ -0,0 +1,5 @@
+
+
+
+
+{% foo %}